Fibrolytic vaccination against ADAM12 reduces desmoplasia in preclinical pancreatic adenocarcinomas.

Cancer-Associated Fibroblasts Immunotherapy Pancreatic Adenocarcinoma Vaccination

Journal

EMBO molecular medicine
ISSN: 1757-4684
Titre abrégé: EMBO Mol Med
Pays: Germany
ID NLM: 101487380

Informations de publication

Date de publication:
30 Oct 2024
Historique:
received: 20 10 2023
accepted: 09 10 2024
revised: 26 09 2024
medline: 31 10 2024
pubmed: 31 10 2024
entrez: 31 10 2024
Statut: aheadofprint

Résumé

A hallmark feature of pancreatic ductal adenocarcinoma (PDAC) is massive intratumoral fibrosis, designated as desmoplasia. Desmoplasia is characterized by the expansion of cancer-associated fibroblasts (CAFs) and a massive increase in extracellular matrix (ECM). During fibrogenesis, distinct genes become reactivated specifically in fibroblasts, e.g., the disintegrin metalloprotease, ADAM12. Previous studies have shown that immunotherapeutic ablation of ADAM12

Identifiants

pubmed: 39478152
doi: 10.1038/s44321-024-00157-4
pii: 10.1038/s44321-024-00157-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : SNF | Swiss National Centre of Competence in Research Kidney Control of Homeostasis (NCCR Kidney.CH)
ID : N-403-06-26 HCP
Organisme : Swiss Cancer League
ID : KFS-4398-02-2018
Organisme : Swiss Cancer League
ID : KFS-5402-08-2021
Organisme : Swiss National Science Fundation
ID : 310030_179235
Organisme : Japan Agency for Medical Research and Development (AMED)
ID : JP23gm6510023
Organisme : University of Zurich
ID : Forschungskredit UZH Postdoc 2019

Informations de copyright

© 2024. The Author(s).

Références

Aghababaei M et al (2013) A disintegrin and metalloproteinase 12 (ADAM12) localizes to invasive trophoblast, promotes cell invasion and directs column outgrowth in early placental development. Mol Hum Reprod 20(3):235–249
doi: 10.1093/molehr/gat084 pubmed: 24243624
Airley RE et al (2003) Glut-1 and CAIX as intrinsic markers of hypoxia in carcinoma of the cervix: relationship to pimonidazole binding. Int J Cancer 104(1):85–91
Cazet AS et al (2018) Targeting stromal remodeling and cancer stem cell plasticity overcomes chemoresistance in triple negative breast cancer. Nat Commun 9(1):2897
doi: 10.1038/s41467-018-05220-6 pubmed: 30042390 pmcid: 6057940
Devaud C et al (2013) Immune modulation of the tumor microenvironment for enhancing cancer immunotherapy. Oncoimmunology 2(8):e25961
Di Carlo SE et al (2023) Depletion of slow-cycling PDGFRα+ADAM12+ mesenchymal cells promotes antitumor immunity by restricting macrophage efferocytosis. Nat Immunol 24(24):1867–1878
Dullaers M, Thielemans K (2006) From pathogen to medicine: HIV-1-derived lentiviral vectors as vehicles for dendritic cell based cancer immunotherapy. J Gene Med 8(1):3–17
Facciponte JG et al (2014) Tumor endothelial marker 1-specific DNA vaccination targets tumor vasculature. J Clin Invest 124(4):1497–1511
Finisguerra V et al (2015) MET is required for the recruitment of anti-tumoural neutrophils. Nature 522(7556):349–353
doi: 10.1038/nature14407 pubmed: 25985180 pmcid: 4594765
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674
doi: 10.1016/j.cell.2011.02.013 pubmed: 21376230
Hegde S et al (2020) Dendritic cell paucity leads to dysfunctional immune surveillance in pancreatic cancer. Cancer Cell 37(3):289–307
Hollingsworth RE, Jansen K (2019) Turning the corner on therapeutic cancer vaccines. npj Vaccines 4(1):1–10
Kalluri R (2016) The biology and function of fibroblasts in cancer. Nat Rev Cancer 16(9):582–598
Krzywinska E et al (2017) Loss of HIF-1α in natural killer cells inhibits tumour growth by stimulating non-productive angiogenesis. Nat Commun 8(1):1597
Lafaro KJ, Melstrom LG (2019) The paradoxical web of pancreatic cancer tumor microenvironment. Am J Pathol 189(1):44–57
doi: 10.1016/j.ajpath.2018.09.009 pubmed: 30558722 pmcid: 6315325
Lynch MD, Watt FM (2018) Fibroblast heterogeneity: implications for human disease. J Clin Invest 128(1):26–35
Olive KP et al (2009) Inhibition of hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324(5933):1457
doi: 10.1126/science.1171362 pubmed: 19460966 pmcid: 2998180
Özdemir BC et al (2014) Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 25(6):719–734
doi: 10.1016/j.ccr.2014.04.005 pubmed: 24856586 pmcid: 4180632
Pereira BA et al (2019) CAF subpopulations: a new reservoir of stromal targets in pancreatic cancer. Trends Cancer 5(11):724–741
doi: 10.1016/j.trecan.2019.09.010 pubmed: 31735290
Pincha M, Sundarasetty BS, Stripecke R (2010) Lentiviral vectors for immunization: an inflammatory field. Expert Rev Vaccines 9(3):309–321
Siegel RL, Miller KD, Jemal A (2016) Cancer statistics, 2016. CA Cancer J Clin 66(1):7–30
doi: 10.3322/caac.21332 pubmed: 26742998
Sobecki M et al (2022) Vaccination-based immunotherapy to target profibrotic cells in liver and lung. Cell Stem Cell 29(10):1459–1474.e9
doi: 10.1016/j.stem.2022.08.012 pubmed: 36113462
Stripecke R (2009) Lentiviral vector-mediated genetic programming of mouse and human dendritic cells. Methods Mol Biol 506:139–158.
Thomas D, Radhakrishnan P (2019) Tumor-stromal crosstalk in pancreatic cancer and tissue fibrosis. Mol Cancer 18(1):14
Uhlig KM et al (2015) Lentiviral protein transfer vectors are an efficient vaccine platform and induce a strong antigen-specific cytotoxic T cell response. J Virol 89(17):9044–9060
Veenstra VL et al (2018) ADAM12 is a circulating marker for stromal activation in pancreatic cancer and predicts response to chemotherapy. Oncogenesis 7(11):87
Vennin C et al (2019) CAF hierarchy driven by pancreatic cancer cell p53-status creates a pro-metastatic and chemoresistant environment via perlecan. Nat Commun 10(1):3637
doi: 10.1038/s41467-019-10968-6 pubmed: 31406163 pmcid: 6691013
Yang X, Jones K, Chen G (2021) Pathology of Pancreatic Ductal Adenocarcinoma. Magy Onkol 65:1–35.
Zhang Y, Zhu L, Wang X (2020) A network-based approach for identification of subtype-specific master regulators in pancreatic ductal adenocarcinoma. Genes 11(2):155

Auteurs

Jing Chen (J)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Michal Sobecki (M)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Ewelina Krzywinska (E)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Kevin Thierry (K)

Cancer Research Center of Lyon, UMR INSERM 1052, CNRS, 5286, Lyon, France.

Mélissa Masmoudi (M)

Cancer Research Center of Lyon, UMR INSERM 1052, CNRS, 5286, Lyon, France.

Shunmugam Nagarajan (S)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Zheng Fan (Z)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Jingyi He (J)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Irina Ferapontova (I)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Eric Nelius (E)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Frauke Seehusen (F)

Laboratory for Animal Model Pathology (LAMP), Institute of Veterinary Pathology, Vetsuisse Faculty, University of Zurich, 8057, Zurich, Switzerland.

Dagmar Gotthardt (D)

Institute of Pharmacology and Toxicology, University of Veterinary Medicine, 1210, Vienna, Austria.

Norihiko Takeda (N)

Department of Cardiovascular Medicine, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.

Lukas Sommer (L)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland.

Veronika Sexl (V)

University of Innsbruck, Innrain 52, 6020, Innsbruck, Austria.

Christian Münz (C)

Viral Immunobiology, Institute of Experimental Immunology, University of Zürich, 8057, Zürich, Switzerland.

David DeNardo (D)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Ana Hennino (A)

Cancer Research Center of Lyon, UMR INSERM 1052, CNRS, 5286, Lyon, France.

Christian Stockmann (C)

University of Zurich, Institute of Anatomy, Winterthurerstrasse 190, CH - 8057, Zurich, Switzerland. christian.stockmann@anatomy.uzh.ch.
Comprehensive Cancer Center Zurich, 8091, Zurich, Switzerland. christian.stockmann@anatomy.uzh.ch.

Classifications MeSH