Single-nucleus and spatial transcriptome profiling of pancreatic cancer identifies multicellular dynamics associated with neoadjuvant treatment.


Journal

Nature genetics
ISSN: 1546-1718
Titre abrégé: Nat Genet
Pays: United States
ID NLM: 9216904

Informations de publication

Date de publication:
08 2022
Historique:
received: 28 08 2021
accepted: 16 06 2022
pubmed: 29 7 2022
medline: 10 8 2022
entrez: 28 7 2022
Statut: ppublish

Résumé

Pancreatic ductal adenocarcinoma (PDAC) is a highly lethal and treatment-refractory cancer. Molecular stratification in pancreatic cancer remains rudimentary and does not yet inform clinical management or therapeutic development. Here, we construct a high-resolution molecular landscape of the cellular subtypes and spatial communities that compose PDAC using single-nucleus RNA sequencing and whole-transcriptome digital spatial profiling (DSP) of 43 primary PDAC tumor specimens that either received neoadjuvant therapy or were treatment naive. We uncovered recurrent expression programs across malignant cells and fibroblasts, including a newly identified neural-like progenitor malignant cell program that was enriched after chemotherapy and radiotherapy and associated with poor prognosis in independent cohorts. Integrating spatial and cellular profiles revealed three multicellular communities with distinct contributions from malignant, fibroblast and immune subtypes: classical, squamoid-basaloid and treatment enriched. Our refined molecular and cellular taxonomy can provide a framework for stratification in clinical trials and serve as a roadmap for therapeutic targeting of specific cellular phenotypes and multicellular interactions.

Identifiants

pubmed: 35902743
doi: 10.1038/s41588-022-01134-8
pii: 10.1038/s41588-022-01134-8
pmc: PMC10290535
mid: NIHMS1901221
doi:

Substances chimiques

Biomarkers, Tumor 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1178-1191

Subventions

Organisme : NCI NIH HHS
ID : K08 CA270417
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA224348
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.

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Auteurs

William L Hwang (WL)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Karthik A Jagadeesh (KA)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Jimmy A Guo (JA)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.
School of Medicine, University of California, San Francisco, San Francisco, CA, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.
Biological and Biomedical Sciences Program, Harvard Medical School, Boston, MA, USA.

Hannah I Hoffman (HI)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
Harvard-MIT MD/PhD and Health Sciences and Technology Program, Harvard Medical School, Boston, MA, USA.

Payman Yadollahpour (P)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Jason W Reeves (JW)

NanoString Technologies, Seattle, WA, USA.

Rahul Mohan (R)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Eugene Drokhlyansky (E)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Nicholas Van Wittenberghe (N)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Orr Ashenberg (O)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Samouil L Farhi (SL)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Denis Schapiro (D)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Laboratory of Systems Pharmacology, Department of Systems Biology, Harvard Medical School, Boston, MA, USA.
Institute for Computational Biomedicine and Institute of Pathology, Faculty of Medicine, Heidelberg University and Heidelberg University Hospital, Heidelberg, Germany.

Prajan Divakar (P)

NanoString Technologies, Seattle, WA, USA.

Eric Miller (E)

NanoString Technologies, Seattle, WA, USA.

Daniel R Zollinger (DR)

NanoString Technologies, Seattle, WA, USA.

George Eng (G)

Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Jason M Schenkel (JM)

Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.

Jennifer Su (J)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Carina Shiau (C)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Patrick Yu (P)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

William A Freed-Pastor (WA)

Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.

Domenic Abbondanza (D)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Arnav Mehta (A)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.
Department of Medical Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Joshua Gould (J)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Conner Lambden (C)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Caroline B M Porter (CBM)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Alexander Tsankov (A)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Danielle Dionne (D)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Julia Waldman (J)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Michael S Cuoco (MS)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Lan Nguyen (L)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Toni Delorey (T)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Devan Phillips (D)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Genentech, South San Francisco, CA, USA.

Jaimie L Barth (JL)

Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Marina Kem (M)

Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Clifton Rodrigues (C)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Debora Ciprani (D)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Jorge Roldan (J)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Piotr Zelga (P)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Vjola Jorgji (V)

Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Jonathan H Chen (JH)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Zackery Ely (Z)

Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Daniel Zhao (D)

New York Medical College, Valhalla, NY, USA.

Kit Fuhrman (K)

NanoString Technologies, Seattle, WA, USA.

Robin Fropf (R)

NanoString Technologies, Seattle, WA, USA.

Joseph M Beechem (JM)

NanoString Technologies, Seattle, WA, USA.

Jay S Loeffler (JS)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

David P Ryan (DP)

Department of Medical Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Colin D Weekes (CD)

Department of Medical Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Cristina R Ferrone (CR)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Motaz Qadan (M)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Martin J Aryee (MJ)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Rakesh K Jain (RK)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Edwin L. Steele Laboratory for Tumor Biology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Donna S Neuberg (DS)

Department of Data Science, Dana-Farber Cancer Institute, Boston, MA, USA.

Jennifer Y Wo (JY)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Theodore S Hong (TS)

Center for Systems Biology and Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Ramnik Xavier (R)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Andrew J Aguirre (AJ)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.

Orit Rozenblatt-Rosen (O)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Genentech, South San Francisco, CA, USA.

Mari Mino-Kenudson (M)

Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Carlos Fernandez-Del Castillo (CF)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Andrew S Liss (AS)

Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

David T Ting (DT)

Department of Medical Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Tyler Jacks (T)

Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA. aviv.regev.sc@gmail.com.

Aviv Regev (A)

Broad Institute of MIT and Harvard, Cambridge, MA, USA. tjacks@mit.edu.
Genentech, South San Francisco, CA, USA. tjacks@mit.edu.

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