Publication date: 25th July 2016
Ductal Carcinoma, the most common form of breast cancer, progresses from noninvasive to invasive when the mammary epithelium invades through the nanoporous basement membrane (BM) into the collagen-rich stromal tissue. Recent studies have demonstrated that tumor cells are capable of both protease-dependent invasion, which is mediated by enzymatic degradation of the extracellular matrix (ECM), and protease-independent invasion, involving cells squeezing through pores. It is thought that proteases are required for BM invasion due to the nanoporosity of the BM. Most of the studies investigating how pore size affects invasion have utilized rigid pores. However, many physiological tissues are viscoelastic, demonstrating both solid and liquid-like properties. Because viscoelastic materials can be malleable, or undergo irreversible deformations due to applied forces, pore size in physiological tissues may not be rigid. Here, we investigated how ECM malleability regulates invasion of the BM. We designed a system of hydrogels, consisting of interpenetrating networks (IPNs) of alginate and reconstituted basement membrane (rBM), in which malleability can be modulated independent of stiffness and ligand density. These IPNs, which present BM ligands and are nanoporous, were then used as substrates for 3D invasion assays with a highly invasive breast cancer cell line (MDA-MB-231). Cells encapsulated in IPNs with low malleability exhibited rounded morphologies and amoeboid blebbing. Cells in IPNs with high malleability were more spread and mesenchymal, and carried out protease-independent invasion into the IPNs with high-aspect ratio, actin-rich protrusions that were mediated through Rac1 activity. Colocalization of actin and β1 integrin-rich plaques in these highly invasive cells further suggests an invadopodial phenotype. In combination, these findings reveal that cells can physically invade through stiff and nanoporous tissues in a protease-independent manner if the tissues are malleable.
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