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PMID: 25979873 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Tumor-Promoting Desmoplasia Is Disrupted by Depleting FAP-Expressing Stromal Cells.

Cancer research ·Vol. 75 ·No. 14 ·2015-07-15 ·Pages 2800-2810

Lo A, Wang LS, Scholler J, Monslow J, Avery D, Newick K, O'Brien S, Evans RA, Bajor DJ, Clendenin C, Durham AC, Buza EL, Vonderheide RH, June CH, Albelda SM, Puré E

Abstract

Malignant cells drive the generation of a desmoplastic and immunosuppressive tumor microenvironment. Cancer-associated stromal cells (CASC) are a heterogeneous population that provides both negative and positive signals for tumor cell growth and metastasis. Fibroblast activation protein (FAP) is a marker of a major subset of CASCs in virtually all carcinomas. Clinically, FAP expression serves as an independent negative prognostic factor for multiple types of human malignancies. Prior studies established that depletion of FAP(+) cells inhibits tumor growth by augmenting antitumor immunity. However, the potential for immune-independent effects on tumor growth have not been defined. Herein, we demonstrate that FAP(+) CASCs are required for maintenance of the provisional tumor stroma because depletion of these cells, by adoptive transfer of FAP-targeted chimeric antigen receptor (CAR) T cells, reduced extracellular matrix proteins and glycosaminoglycans. Adoptive transfer of FAP-CAR T cells also decreased tumor vascular density and restrained growth of desmoplastic human lung cancer xenografts and syngeneic murine pancreatic cancers in an immune-independent fashion. Adoptive transfer of FAP-CAR T cells also restrained autochthonous pancreatic cancer growth. These data distinguish the function of FAP(+) CASCs from other CASC subsets and provide support for further development of FAP(+) stromal cell-targeted therapies for the treatment of solid tumors.

MeSH Terms
Animals Endopeptidases Epithelial-Mesenchymal Transition/genetics Extracellular Matrix/pathology Gelatinases/genetics,metabolism Humans Membrane Proteins/genetics,metabolism Mice Mice, Inbred C57BL Mice, Inbred NOD Mice, Knockout Mice, SCID Neoplasms/immunology,pathology Serine Endopeptidases/genetics,metabolism Stromal Cells/metabolism,physiology Tumor Cells, Cultured Tumor Microenvironment/physiology
Chemicals
Membrane Proteins Endopeptidases Serine Endopeptidases fibroblast activation protein alpha Gelatinases
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Lo Albert
Department of Biomedical Sciences, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Cell and Molecular Biology Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Wang Liang-Chuan S
Thoracic Oncology Research Laboratory, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Scholler John
Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Monslow James
Department of Biomedical Sciences, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Avery Diana
Department of Biomedical Sciences, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Newick Kheng
Thoracic Oncology Research Laboratory, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
O'Brien Shaun
Thoracic Oncology Research Laboratory, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Evans Rebecca A
Cell and Molecular Biology Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Bajor David J
Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Clendenin Cynthia
Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Durham Amy C
Department of Pathobiology, School of Veterinary Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Buza Elizabeth L
Department of Pathobiology, School of Veterinary Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Vonderheide Robert H
Cell and Molecular Biology Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
June Carl H
Cell and Molecular Biology Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Albelda Steven M
Cell and Molecular Biology Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Thoracic Oncology Research Laboratory, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
Puré Ellen
Department of Biomedical Sciences, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Cell and Molecular Biology Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania. | Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
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Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2015-07-15
Epub
2015-00-15
Pages
2800-2810
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC4506263
Subset
IM
Grants
NCI NIH HHS · P01 CA066726 · United States
NCI NIH HHS · R01 CA141144 · United States
NCI NIH HHS · R01 CA169123 · United States
NCI NIH HHS · P30 CA016520 · United States
NHLBI NIH HHS · T32 HL007775 · United States
NCI NIH HHS · R21 CA169741 · United States
NCI NIH HHS · P01 CA 66726-07 · United States
NCI NIH HHS · R01 CA 172921 · United States
NCI NIH HHS · R01 CA172921 · United States
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