Spatially Resolved Multi-Omics Single-Cell Analyses Inform Mechanisms of Immune Dysfunction in Pancreatic Cancer.


Journal

Gastroenterology
ISSN: 1528-0012
Titre abrégé: Gastroenterology
Pays: United States
ID NLM: 0374630

Informations de publication

Date de publication:
10 2023
Historique:
received: 14 08 2022
revised: 22 05 2023
accepted: 23 05 2023
medline: 25 9 2023
pubmed: 2 6 2023
entrez: 1 6 2023
Statut: ppublish

Résumé

As pancreatic ductal adenocarcinoma (PDAC) continues to be recalcitrant to therapeutic interventions, including poor response to immunotherapy, albeit effective in other solid malignancies, a more nuanced understanding of the immune microenvironment in PDAC is urgently needed. We aimed to unveil a detailed view of the immune micromilieu in PDAC using a spatially resolved multimodal single-cell approach. We applied single-cell RNA sequencing, spatial transcriptomics, multiplex immunohistochemistry, and mass cytometry to profile the immune compartment in treatment-naïve PDAC tumors and matched adjacent normal pancreatic tissue, as well as in the systemic circulation. We determined prognostic associations of immune signatures and performed a meta-analysis of the immune microenvironment in PDAC and lung adenocarcinoma on single-cell level. We provided a spatially resolved fine map of the immune landscape in PDAC. We substantiated the exhausted phenotype of CD8 T cells and immunosuppressive features of myeloid cells, and highlighted immune subsets with potentially underappreciated roles in PDAC that diverged from immune populations within adjacent normal areas, particularly CD4 T cell subsets and natural killer T cells that are terminally exhausted and acquire a regulatory phenotype. Differential analysis of immune phenotypes in PDAC and lung adenocarcinoma revealed the presence of extraordinarily immunosuppressive subtypes in PDAC, along with a distinctive immune checkpoint composition. Our study sheds light on the multilayered immune dysfunction in PDAC and presents a holistic view of the immune landscape in PDAC and lung adenocarcinoma, providing a comprehensive resource for functional studies and the exploration of therapeutically actionable targets in PDAC.

Sections du résumé

BACKGROUND & AIMS
As pancreatic ductal adenocarcinoma (PDAC) continues to be recalcitrant to therapeutic interventions, including poor response to immunotherapy, albeit effective in other solid malignancies, a more nuanced understanding of the immune microenvironment in PDAC is urgently needed. We aimed to unveil a detailed view of the immune micromilieu in PDAC using a spatially resolved multimodal single-cell approach.
METHODS
We applied single-cell RNA sequencing, spatial transcriptomics, multiplex immunohistochemistry, and mass cytometry to profile the immune compartment in treatment-naïve PDAC tumors and matched adjacent normal pancreatic tissue, as well as in the systemic circulation. We determined prognostic associations of immune signatures and performed a meta-analysis of the immune microenvironment in PDAC and lung adenocarcinoma on single-cell level.
RESULTS
We provided a spatially resolved fine map of the immune landscape in PDAC. We substantiated the exhausted phenotype of CD8 T cells and immunosuppressive features of myeloid cells, and highlighted immune subsets with potentially underappreciated roles in PDAC that diverged from immune populations within adjacent normal areas, particularly CD4 T cell subsets and natural killer T cells that are terminally exhausted and acquire a regulatory phenotype. Differential analysis of immune phenotypes in PDAC and lung adenocarcinoma revealed the presence of extraordinarily immunosuppressive subtypes in PDAC, along with a distinctive immune checkpoint composition.
CONCLUSIONS
Our study sheds light on the multilayered immune dysfunction in PDAC and presents a holistic view of the immune landscape in PDAC and lung adenocarcinoma, providing a comprehensive resource for functional studies and the exploration of therapeutically actionable targets in PDAC.

Identifiants

pubmed: 37263303
pii: S0016-5085(23)00810-7
doi: 10.1053/j.gastro.2023.05.036
pii:
doi:

Types de publication

Meta-Analysis Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

891-908.e14

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Suhail Yousuf (S)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Mengjie Qiu (M)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Lena Voith von Voithenberg (L)

Division of Applied Bioinformatics, German Cancer Research Center, Heidelberg, Germany.

Johannes Hulkkonen (J)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Igor Macinkovic (I)

Institute of Biochemistry I, Faculty of Medicine, Goethe-University Frankfurt, Frankfurt, Germany.

Axel R Schulz (AR)

German Rheumatism Research Center, Berlin, Germany.

Domenic Hartmann (D)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Florian Mueller (F)

Division of Chronic Inflammation and Cancer, German Cancer Research Center, Heidelberg, Germany.

Margarete Mijatovic (M)

Institute of Biochemistry I, Faculty of Medicine, Goethe-University Frankfurt, Frankfurt, Germany.

David Ibberson (D)

Deep Sequencing Core Facility, BioQuant, Heidelberg University, Heidelberg, Germany.

Karam T AlHalabi (KT)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Jenny Hetzer (J)

Division of Chronic Inflammation and Cancer, German Cancer Research Center, Heidelberg, Germany.

Simon Anders (S)

BioQuant Center, Heidelberg University, Heidelberg, Germany.

Bernhard Brüne (B)

Institute of Biochemistry I, Faculty of Medicine, Goethe-University Frankfurt, Frankfurt, Germany; Frankfurt Cancer Institute, Goethe-University Frankfurt, Frankfurt, Germany; German Cancer Consortium, Partner Site Frankfurt, Germany.

Henrik E Mei (HE)

German Rheumatism Research Center, Berlin, Germany.

Charles D Imbusch (CD)

Division of Applied Bioinformatics, German Cancer Research Center, Heidelberg, Germany.

Benedikt Brors (B)

Division of Applied Bioinformatics, German Cancer Research Center, Heidelberg, Germany.

Mathias Heikenwälder (M)

Division of Chronic Inflammation and Cancer, German Cancer Research Center, Heidelberg, Germany.

Matthias M Gaida (MM)

Institute of Pathology, University Medical Center Mainz, Johannes Gutenberg University, Mainz, Germany; Research Center for Immunotherapy, University Medical Center Mainz, Johannes Gutenberg University, Mainz, Germany; Joint Unit Immunopathology, Institute of Pathology, University Medical Center, Johannes Gutenberg University and Translational Oncology, University Medical Center Mainz, Mainz, Germany.

Markus W Büchler (MW)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Andreas Weigert (A)

Institute of Biochemistry I, Faculty of Medicine, Goethe-University Frankfurt, Frankfurt, Germany; Frankfurt Cancer Institute, Goethe-University Frankfurt, Frankfurt, Germany; German Cancer Consortium, Partner Site Frankfurt, Germany.

Thilo Hackert (T)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Susanne Roth (S)

Department of Surgery, Heidelberg University Hospital, Heidelberg, Germany. Electronic address: susanne.roth@med.uni-heidelberg.de.

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Classifications MeSH