PUBLICATION

A high-content screen identifies drugs that restrict tumor cell extravasation across the endothelial barrier

Authors
Hilfenhaus, G., Mompeón, A., Freshman, J., Prajapati, D., Hernandez, G., Freitas, V.M., Ma, F., Langenbacher, A.D., Mirkov, S., Song, D., Cho, B.K., Goo, Y.A., Pellegrini, M., Chen, J.N., Damoiseaux, R., Iruela-Arispe, M.L.
ID
ZDB-PUB-201123-4
Date
2020
Source
Cancer research   81(3): 619-633 (Journal)
Registered Authors
Keywords
none
MeSH Terms
  • Proteomics
  • Transendothelial and Transepithelial Migration/drug effects*
  • Cell Proliferation
  • Animals
  • Zebrafish
  • Cell Line, Tumor
  • Cell Communication/drug effects
  • Kininogens/analysis
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Mice, Inbred C57BL
  • Endothelial Cells/drug effects
  • Mice
  • Colforsin/pharmacology*
  • Mice, Inbred BALB C
  • Metabolomics
  • Neoplasm Invasiveness
  • Niclosamide/pharmacology*
  • Drug Screening Assays, Antitumor/methods
  • Lung Neoplasms/pathology*
  • Female
  • Endothelium, Vascular*/drug effects
  • Male
  • Neoplastic Cells, Circulating*
PubMed
33218969 Full text @ Cancer Res.
Abstract
Metastases largely rely on hematogenous dissemination of tumor cells via the vascular system and significantly limit prognosis of patients with solid tumors. To colonize distant sites, circulating tumor cells must destabilize the endothelial barrier and transmigrate across the vessel wall. Here we performed a high-content screen to identify drugs that block tumor cell extravasation by testing 3520 compounds on a transendothelial invasion co-culture assay. Hits were further characterized and validated using a series of in vitro assays, a zebrafish model enabling 3-D visualization of tumor cell extravasation, and mouse models of lung metastasis. The initial screen advanced 38 compounds as potential hits, of which 4 compounds enhanced endothelial barrier stability while concurrently suppressing tumor cell motility. Two compounds niclosamide and forskolin significantly reduced tumor cell extravasation in zebrafish, and niclosamide drastically impaired metastasis in mice. Because niclosamide had not previously been linked with effects on barrier function, single cell RNA sequencing uncovered mechanistic effects of the drug on both tumor and endothelial cells. Importantly, niclosamide affected homotypic and heterotypic signaling critical to intercellular junctions, cell-matrix interactions, and cytoskeletal regulation. Proteomic analysis indicated that niclosamide-treated mice also showed reduced levels of kininogen, the precursor to the permeability mediator bradykinin. Our findings designate niclosamide as an effective drug that restricts tumor cell extravasation through modulation of signaling pathways, chemokines, and tumor-endothelial cell interactions.
Genes / Markers
Figures
Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping