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Article ; Online: Transcriptional space-time mapping identifies concerted immune and stromal cell patterns and gene programs in wound healing and cancer.

Hu, Kenneth H / Kuhn, Nicholas F / Courau, Tristan / Tsui, Jessica / Samad, Bushra / Ha, Patrick / Kratz, Johannes R / Combes, Alexis J / Krummel, Matthew F

Cell stem cell

2023 Volume 30, Issue 6, Page(s) 885–903.e10

Abstract: Tissue repair responses in metazoans are highly coordinated by different cell types over space and time. However, comprehensive single-cell-based characterization covering this coordination is lacking. Here, we captured transcriptional states of single ... ...

Abstract	Tissue repair responses in metazoans are highly coordinated by different cell types over space and time. However, comprehensive single-cell-based characterization covering this coordination is lacking. Here, we captured transcriptional states of single cells over space and time during skin wound closure, revealing choreographed gene-expression profiles. We identified shared space-time patterns of cellular and gene program enrichment, which we call multicellular "movements" spanning multiple cell types. We validated some of the discovered space-time movements using large-volume imaging of cleared wounds and demonstrated the value of this analysis to predict "sender" and "receiver" gene programs in macrophages and fibroblasts. Finally, we tested the hypothesis that tumors are like "wounds that never heal" and found conserved wound healing movements in mouse melanoma and colorectal tumor models, as well as human tumor samples, revealing fundamental multicellular units of tissue biology for integrative studies.
MeSH term(s)	Mice ; Animals ; Humans ; Wound Healing/genetics ; Skin/pathology ; Neoplasms/pathology ; Macrophages/metabolism ; Fibroblasts/physiology ; Stromal Cells
Language	English
Publishing date	2023-06-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2375354-7
ISSN	1875-9777 ; 1934-5909
ISSN (online)	1875-9777
ISSN	1934-5909
DOI	10.1016/j.stem.2023.05.001
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Article ; Online: Activating Immune Recognition in Pancreatic Ductal Adenocarcinoma via Autophagy Inhibition, MEK Blockade, and CD40 Agonism.

Jiang, Honglin / Courau, Tristan / Borison, Joseph / Ritchie, Alexa J / Mayer, Aaron T / Krummel, Matthew F / Collisson, Eric A

Gastroenterology

2021 Volume 162, Issue 2, Page(s) 590–603.e14

Abstract: Background and aims: Patients with pancreatic ductal adenocarcinoma (PDA) have not yet benefitted from the revolution in cancer immunotherapy due in large part to a dominantly immunosuppressive tumor microenvironment. MEK inhibition combined with ... ...

Abstract	Background and aims: Patients with pancreatic ductal adenocarcinoma (PDA) have not yet benefitted from the revolution in cancer immunotherapy due in large part to a dominantly immunosuppressive tumor microenvironment. MEK inhibition combined with autophagy inhibition leads to transient tumor responses in some patients with PDA. We examined the functional effects of combined MEK and autophagy inhibition on the PDA immune microenvironment and the synergy of combined inhibition of MEK and autophagy with CD40 agonism (aCD40) against PDA using immunocompetent model systems. Methods: We implanted immunologically "cold" murine PDA cells orthotopically in wide type C57BL/6J mice. We administered combinations of inhibitors of MEK1/2, inhibitors of autophagy, and aCD40 and measured anticancer efficacy and immune sequelae using mass cytometry and multiplexed immunofluorescence imaging analysis to characterize the tumor microenvironment. We also used human and mouse PDA cell lines and human macrophages in vitro to perform functional assays to elucidate the cellular effects induced by the treatments. Results: We find that coinhibition of MEK (using cobimetinib) and autophagy (using mefloquine), but not either treatment alone, activates the STING/type I interferon pathway in tumor cells that in turn activates paracrine tumor associated macrophages toward an immunogenic M1-like phenotype. This switch is further augmented by aCD40. Triple therapy (cobimetinib + mefloquine + aCD40) achieved cytotoxic T-cell activation in an immunologically "cold" mouse PDA model, leading to enhanced antitumor immunity. Conclusions: MEK and autophagy coinhibition coupled with aCD40 invokes immune repolarization and is an attractive therapeutic approach for PDA immunotherapy development.
MeSH term(s)	Animals ; Autophagy/drug effects ; Autophagy/immunology ; Azetidines/pharmacology ; CD40 Antigens/agonists ; Carcinoma, Pancreatic Ductal/immunology ; Cell Line, Tumor ; Drug Synergism ; Humans ; Hydroxychloroquine/pharmacology ; Immunotherapy ; Interferon Type I/drug effects ; Interferon Type I/immunology ; MAP Kinase Kinase 1/antagonists & inhibitors ; MAP Kinase Kinase 2/antagonists & inhibitors ; Macrophages ; Mefloquine/pharmacology ; Membrane Proteins/drug effects ; Membrane Proteins/immunology ; Mice ; Pancreatic Neoplasms/immunology ; Paracrine Communication/drug effects ; Paracrine Communication/immunology ; Piperidines/pharmacology ; Protein Kinase Inhibitors/pharmacology ; Tumor Escape ; Tumor Microenvironment/drug effects ; Tumor Microenvironment/immunology ; Tumor-Associated Macrophages/drug effects ; Tumor-Associated Macrophages/immunology
Chemical Substances	Azetidines ; CD40 Antigens ; Interferon Type I ; Membrane Proteins ; Piperidines ; Protein Kinase Inhibitors ; STING1 protein, human ; Sting1 protein, mouse ; Hydroxychloroquine (4QWG6N8QKH) ; MAP Kinase Kinase 1 (EC 2.7.12.2) ; MAP Kinase Kinase 2 (EC 2.7.12.2) ; cobimetinib (ER29L26N1X) ; Mefloquine (TML814419R)
Language	English
Publishing date	2021-10-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80112-4
ISSN	1528-0012 ; 0016-5085
ISSN (online)	1528-0012
ISSN	0016-5085
DOI	10.1053/j.gastro.2021.09.066
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Article ; Online: Tumor-associated macrophage heterogeneity is driven by tissue territories in breast cancer.

Laviron, Marie / Petit, Maxime / Weber-Delacroix, Eléonore / Combes, Alexis J / Arkal, Arjun Rao / Barthélémy, Sandrine / Courau, Tristan / Hume, David A / Combadière, Christophe / Krummel, Matthew F / Boissonnas, Alexandre

Cell reports

2022 Volume 39, Issue 8, Page(s) 110865

Abstract: Tissue-resident macrophages adapt to local signals within tissues to acquire specific functions. Neoplasia transforms the tissue, raising the question as to how the environmental perturbations contribute to tumor-associated macrophage (TAM) identity and ... ...

Abstract	Tissue-resident macrophages adapt to local signals within tissues to acquire specific functions. Neoplasia transforms the tissue, raising the question as to how the environmental perturbations contribute to tumor-associated macrophage (TAM) identity and functions. Combining single-cell RNA sequencing (scRNA-seq) with spatial localization of distinct TAM subsets by imaging, we discover that TAM transcriptomic programs follow two main differentiation paths according to their localization in the stroma or in the neoplastic epithelium of the mammary duct. Furthermore, this diversity is exclusively detected in a spontaneous tumor model and tracks the different tissue territories as well as the type of tumor lesion. These TAM subsets harbor distinct capacity to activate CD8+ T cells and phagocyte tumor cells, supporting that specific tumor regions, rather than defined activation states, are the major drivers of TAM plasticity and heterogeneity. The distinctions created here provide a framework to design cancer treatment targeting specific TAM niches.
MeSH term(s)	Breast Neoplasms/genetics ; Breast Neoplasms/pathology ; Female ; Humans ; Macrophages/pathology ; Transcriptome/genetics ; Tumor-Associated Macrophages
Language	English
Publishing date	2022-05-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2022.110865
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Article: Cyclone: an accessible pipeline to analyze, evaluate and optimize multiparametric cytometry data.

bioRxiv : the preprint server for biology

2023

Abstract: In the past decade, high-dimensional single cell technologies have revolutionized basic and translational immunology research and are now a key element of the toolbox used by scientists to study the immune system. However, analysis of the data generated ... ...

Abstract	In the past decade, high-dimensional single cell technologies have revolutionized basic and translational immunology research and are now a key element of the toolbox used by scientists to study the immune system. However, analysis of the data generated by these approaches often requires clustering algorithms and dimensionality reduction representation which are computationally intense and difficult to evaluate and optimize. Here we present Cyclone, an analysis pipeline integrating dimensionality reduction, clustering, evaluation and optimization of clustering resolution, and downstream visualization tools facilitating the analysis of a wide range of cytometry data. We benchmarked and validated Cyclone on mass cytometry (CyTOF), full spectrum fluorescence-based cytometry, and multiplexed immunofluorescence (IF) in a variety of biological contexts, including infectious diseases and cancer. In each instance, Cyclone not only recapitulates gold standard immune cell identification, but also enables the unsupervised identification of lymphocytes and mononuclear phagocytes subsets that are associated with distinct biological features. Altogether, the Cyclone pipeline is a versatile and accessible pipeline for performing, optimizing, and evaluating clustering on variety of cytometry datasets which will further power immunology research and provide a scaffold for biological discovery.
Language	English
Publishing date	2023-03-11
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.08.531782
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Article ; Online: Cyclone: an accessible pipeline to analyze, evaluate, and optimize multiparametric cytometry data.

Frontiers in immunology

2023 Volume 14, Page(s) 1167241

Abstract: In the past decade, high-dimensional single-cell technologies have revolutionized basic and translational immunology research and are now a key element of the toolbox used by scientists to study the immune system. However, analysis of the data generated ... ...

Abstract	In the past decade, high-dimensional single-cell technologies have revolutionized basic and translational immunology research and are now a key element of the toolbox used by scientists to study the immune system. However, analysis of the data generated by these approaches often requires clustering algorithms and dimensionality reduction representation, which are computationally intense and difficult to evaluate and optimize. Here, we present Cytometry Clustering Optimization and Evaluation (Cyclone), an analysis pipeline integrating dimensionality reduction, clustering, evaluation, and optimization of clustering resolution, and downstream visualization tools facilitating the analysis of a wide range of cytometry data. We benchmarked and validated Cyclone on mass cytometry (CyTOF), full-spectrum fluorescence-based cytometry, and multiplexed immunofluorescence (IF) in a variety of biological contexts, including infectious diseases and cancer. In each instance, Cyclone not only recapitulates gold standard immune cell identification but also enables the unsupervised identification of lymphocytes and mononuclear phagocyte subsets that are associated with distinct biological features. Altogether, the Cyclone pipeline is a versatile and accessible pipeline for performing, optimizing, and evaluating clustering on a variety of cytometry datasets, which will further power immunology research and provide a scaffold for biological discovery.
MeSH term(s)	Cyclonic Storms ; Algorithms ; Benchmarking ; Cluster Analysis ; Technology
Language	English
Publishing date	2023-09-04
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2023.1167241
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Article ; Online: Correction: Activated dendritic cells modulate proliferation and differentiation of human myoblasts.

Ladislau, Leandro / Portilho, Débora M / Courau, Tristan / Solares-Pérez, Alhondra / Negroni, Elisa / Lainé, Jeanne / Klatzmann, David / Bonomo, Adriana / Allenbach, Yves / Benveniste, Olivier / Riederer, Ingo / Savino, Wilson / Mouly, Vincent / Butler-Browne, Gillian / Benjamim, Claudia F

Cell death & disease

2022 Volume 13, Issue 9, Page(s) 811

Language	English
Publishing date	2022-09-22
Publishing country	England
Document type	Published Erratum
ZDB-ID	2541626-1
ISSN	2041-4889 ; 2041-4889
ISSN (online)	2041-4889
ISSN	2041-4889
DOI	10.1038/s41419-022-05278-7
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Article ; Online: Spatiotemporal co-dependency between macrophages and exhausted CD8

Kersten, Kelly / Hu, Kenneth H / Combes, Alexis J / Samad, Bushra / Harwin, Tory / Ray, Arja / Rao, Arjun Arkal / Cai, En / Marchuk, Kyle / Artichoker, Jordan / Courau, Tristan / Shi, Quanming / Belk, Julia / Satpathy, Ansuman T / Krummel, Matthew F

Cancer cell

2022 Volume 40, Issue 6, Page(s) 624–638.e9

Abstract: T cell exhaustion is a major impediment to antitumor immunity. However, it remains elusive how other immune cells in the tumor microenvironment (TME) contribute to this dysfunctional state. Here, we show that the biology of tumor-associated macrophages ( ... ...

Abstract	T cell exhaustion is a major impediment to antitumor immunity. However, it remains elusive how other immune cells in the tumor microenvironment (TME) contribute to this dysfunctional state. Here, we show that the biology of tumor-associated macrophages (TAMs) and exhausted T cells (T
MeSH term(s)	CD8-Positive T-Lymphocytes ; Cell Differentiation ; Humans ; Macrophages ; Neoplasms/genetics ; Tumor Microenvironment
Language	English
Publishing date	2022-05-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2078448-X
ISSN	1878-3686 ; 1535-6108
ISSN (online)	1878-3686
ISSN	1535-6108
DOI	10.1016/j.ccell.2022.05.004
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Article ; Online: Regulatory T Cells Orchestrate Similar Immune Evasion of Fetuses and Tumors in Mice.

Nehar-Belaid, Djamel / Courau, Tristan / Dérian, Nicolas / Florez, Laura / Ruocco, Maria Grazia / Klatzmann, David

Journal of immunology (Baltimore, Md. : 1950)

2016 Volume 196, Issue 2, Page(s) 678–690

Abstract: Embryos and tumors are both masses of dividing cells expressing foreign Ags, but they are not rejected by the immune system. We hypothesized that similar tolerogenic mechanisms prevent their rejection. Global comparison of fetal and tumor ... ...

Abstract	Embryos and tumors are both masses of dividing cells expressing foreign Ags, but they are not rejected by the immune system. We hypothesized that similar tolerogenic mechanisms prevent their rejection. Global comparison of fetal and tumor microenvironments through transcriptomics in mice revealed strikingly similar and dramatic decreases in expression of numerous immune-related pathways, including Ag presentation and T cell signaling. Unsupervised analyses highlighted the parallel kinetics and similarities of immune signature downregulation, from the very first days after tumor or embryo implantation. Besides upregulated signatures related to cell proliferation, the only significant signatures shared by the two conditions across all biological processes and all time points studied were downmodulated immune response signatures. Regulatory T cell depletion completely reverses this immune downmodulation to an immune upregulation that leads to fetal or tumor immune rejection. We propose that evolutionarily selected mechanisms that protect mammalian fetuses from immune attack are hijacked to license tumor development.
MeSH term(s)	Animals ; Female ; Fetal Development/immunology ; Fetus/immunology ; Immune Tolerance/immunology ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Neoplasms/immunology ; T-Lymphocytes, Regulatory/immunology ; Transcriptome ; Tumor Escape/immunology
Language	English
Publishing date	2016-01-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.1501834
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Article ; Online: KLRG1 and CD103 Expressions Define Distinct Intestinal Tissue-Resident Memory CD8 T Cell Subsets Modulated in Crohn's Disease.

Bottois, Hugo / Ngollo, Marjolaine / Hammoudi, Nassim / Courau, Tristan / Bonnereau, Julie / Chardiny, Victor / Grand, Céline / Gergaud, Brice / Allez, Matthieu / Le Bourhis, Lionel

Frontiers in immunology

2020 Volume 11, Page(s) 896

Abstract: Intestinal tissue-resident memory CD8 T cells (Trm) are non-recirculating effector cells ideally positioned to detect and react to microbial infections in the gut mucosa. There is an emerging understanding of Trm cell differentiation and functions, but ... ...

Abstract	Intestinal tissue-resident memory CD8 T cells (Trm) are non-recirculating effector cells ideally positioned to detect and react to microbial infections in the gut mucosa. There is an emerging understanding of Trm cell differentiation and functions, but their implication in inflammatory bowel diseases, such as Crohn's disease (CD), is still unknown. Here, we describe CD8 cells in the human intestine expressing KLRG1 or CD103, two receptors of E-cadherin. While CD103 CD8 T cells are present in high numbers in the mucosa of CD patients and controls, KLRG1 CD8 T cells are increased in inflammatory conditions. Mucosal CD103 CD8 T cells are more responsive to TCR restimulation, but KLRG1 CD8 T cells show increased cytotoxic and proliferative potential. CD103 CD8 T cells originate mostly from KLRG1 negative cells after TCR triggering and TGFβ stimulation. Interestingly, mucosal CD103 CD8 T cells from CD patients display major changes in their transcriptomic landscape compared to controls. They express Th17 related genes including CCL20, IL22, and IL26, which could contribute to the pathogenesis of CD. Overall, these findings suggest that CD103 CD8 T cells in CD induce a tissue-wide alert increasing innate immune responses and recruitment of effector cells such as KLRG1 CD8 T cells.
MeSH term(s)	Antigens, CD/metabolism ; CD8-Positive T-Lymphocytes/classification ; CD8-Positive T-Lymphocytes/immunology ; Clinical Trials as Topic ; Crohn Disease/immunology ; Crohn Disease/physiopathology ; Gene Expression Profiling ; Humans ; Immunity, Innate ; Immunologic Memory ; Inflammation ; Integrin alpha Chains/metabolism ; Interleukins/immunology ; Intestinal Mucosa/immunology ; Lectins, C-Type/metabolism ; Receptors, Immunologic/metabolism ; T-Lymphocyte Subsets/immunology
Chemical Substances	Antigens, CD ; Integrin alpha Chains ; Interleukins ; KLRG1 protein, human ; Lectins, C-Type ; Receptors, Immunologic ; alpha E integrins
Language	English
Publishing date	2020-05-12
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2020.00896
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Article ; Online: Autologous T cell responses to primary human colorectal cancer spheroids are enhanced by ectonucleotidase inhibition.

Gut

2022 Volume 72, Issue 4, Page(s) 699–709

Abstract: Objective: T cells are major effectors of the antitumoural immune response. Their activation by tumour-associated antigens can unleash their proliferation and cytotoxic functions, leading to tumour cell elimination. However, tumour-related ... ...

Abstract	Objective: T cells are major effectors of the antitumoural immune response. Their activation by tumour-associated antigens can unleash their proliferation and cytotoxic functions, leading to tumour cell elimination. However, tumour-related immunosuppressive mechanisms including the overexpression of immune checkpoints like programmed cell death protein-1 (PD-1), are also engaged, promoting immune escape. Current immunotherapies targeting these pathways have demonstrated weak efficacy in colorectal cancer (CRC). It is thus crucial to find new targets for immunotherapy in this cancer type. Design: In a prospective cohort of patients with CRC, we investigated the phenotype of tumour-related and non-tumour related intestinal T cells (n=44), particularly the adenosinergic pathway, correlating with clinical phenotype. An autologous coculture model was developed between patient-derived primary tumour spheroids and their autologous tumour-associated lymphocytes. We used this relevant model to assess the effects of CD39 blockade on the antitumour T cell response. Results: We show the increased expression of CD39, and its co-expression with PD-1, on tumour infiltrating T cells compared with mucosal lymphocytes. CD39 expression was higher in the right colon and early-stage tumours, thus defining a subset of patients potentially responsive to CD39 blockade. Finally, we demonstrate in autologous conditions that CD39 blockade triggers T cell infiltration and tumour spheroid destruction in cocultures. Conclusion: In CRC, CD39 is strongly expressed on tumour infiltrating lymphocytes and its inhibition represents a promising therapeutic strategy for treating patients.
MeSH term(s)	Humans ; T-Lymphocytes ; Programmed Cell Death 1 Receptor/metabolism ; Prospective Studies ; Intestines/pathology ; Colorectal Neoplasms/pathology
Chemical Substances	Programmed Cell Death 1 Receptor
Language	English
Publishing date	2022-07-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80128-8
ISSN	1468-3288 ; 0017-5749
ISSN (online)	1468-3288
ISSN	0017-5749
DOI	10.1136/gutjnl-2021-326553
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