Document Detail


Breast cancer subtype-specific interactions with the microenvironment dictate mechanisms of invasion.
MedLine Citation:
PMID:  21908556     Owner:  NLM     Status:  MEDLINE    
Abstract/OtherAbstract:
Most ductal breast carcinoma cells are weakly invasive in vitro and in vivo, suggesting that components of their microenvironment may facilitate a transition from in situ to invasive stages during progression. Here, we report that coculture of mammary fibroblasts specifically triggers invasive behavior in basal-type breast cancer cells through a ligand independent mechanism. When cultured alone in organotypic culture, both basal- and luminal-type breast cancer cells formed noninvasive spheroids with characteristics of ductal carcinoma in situ (DCIS). In contrast, when cocultured with mammary fibroblasts, basal-type spheroids exhibited invasive character whereas the luminal-type spheroids retained a benign and noninvasive duct-like architecture. Real-time imaging and functional studies revealed that the specificity of invasion was linked to a unique capacity of basal-type breast cancer cells to move within spheroids. Mammary fibroblasts induced invasion by triggering basal-type breast cancer cells to convert from a noninvasive program of mammary epithelial morphogenesis to an invasive program of sprouting endothelial angiogenesis. Contrary to the existing invasion models, soluble ligands produced by the fibroblasts were not sufficient to trigger invasion. Instead, basal-type invasion relied upon a Cdc42-dependent reorganization of collagen fibers in the extracellular matrix by fibroblasts. Inhibiting basal-type cell movement with clinically relevant drugs blocked invasion both in organotypic culture and in animals, suggesting a new treatment strategy for early-stage patients. Together our findings establish that fibroblast recruitment by basal-type breast cancer cells into early-stage tumors is sufficient to trigger their conversion from a benign, noninvasive DCIS-like stage to a malignant invasive stage. Furthermore, our findings suggest that different subtypes of breast cancer may require distinct types of contributions from the microenvironment to undergo malignant progression.
Authors:
Tuyen T Dang; Amanda M Prechtl; Gray W Pearson
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Publication Detail:
Type:  Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't     Date:  2011-09-09
Journal Detail:
Title:  Cancer research     Volume:  71     ISSN:  1538-7445     ISO Abbreviation:  Cancer Res.     Publication Date:  2011 Nov 
Date Detail:
Created Date:  2011-11-01     Completed Date:  2012-01-09     Revised Date:  2013-02-19    
Medline Journal Info:
Nlm Unique ID:  2984705R     Medline TA:  Cancer Res     Country:  United States    
Other Details:
Languages:  eng     Pagination:  6857-66     Citation Subset:  IM    
Copyright Information:
©2011 AACR.
Affiliation:
Harold C. Simmons Comprehensive Cancer Center and the Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
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MeSH Terms
Descriptor/Qualifier:
Animals
Breast / cytology
Breast Neoplasms / classification,  pathology*
Carcinoma, Ductal, Breast / classification,  pathology*
Carcinoma, Intraductal, Noninfiltrating / pathology*
Cell Movement / drug effects,  physiology
Cells, Cultured / cytology,  physiology
Coculture Techniques
Collagen / physiology
Culture Media, Conditioned / pharmacology
Extracellular Matrix / physiology,  ultrastructure
Female
Fibroblasts / cytology,  physiology
Humans
Mice
Mice, SCID
Neoplasm Invasiveness / physiopathology*,  prevention & control
Neoplasm Transplantation
Neovascularization, Pathologic / pathology
Protein Kinase Inhibitors / pharmacology
RNA, Small Interfering / pharmacology
Spheroids, Cellular / physiology,  transplantation
Tumor Cells, Cultured / cytology,  drug effects,  physiology
Tumor Microenvironment / physiology*
cdc42 GTP-Binding Protein / antagonists & inhibitors,  genetics,  physiology
Grant Support
ID/Acronym/Agency:
1R01CA155241/CA/NCI NIH HHS; 5T32CA124334-04/CA/NCI NIH HHS; R01 CA155241-01/CA/NCI NIH HHS; UL1-RR024982/RR/NCRR NIH HHS
Chemical
Reg. No./Substance:
0/Culture Media, Conditioned; 0/Protein Kinase Inhibitors; 0/RNA, Small Interfering; 9007-34-5/Collagen; EC 3.6.5.2/cdc42 GTP-Binding Protein
Comments/Corrections

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