Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis

J Cell Biol. 2003 Jan 20;160(2):267-77. doi: 10.1083/jcb.200209006. Epub 2003 Jan 13.

Abstract

Invasive tumor dissemination in vitro and in vivo involves the proteolytic degradation of ECM barriers. This process, however, is only incompletely attenuated by protease inhibitor-based treatment, suggesting the existence of migratory compensation strategies. In three-dimensional collagen matrices, spindle-shaped proteolytically potent HT-1080 fibrosarcoma and MDA-MB-231 carcinoma cells exhibited a constitutive mesenchymal-type movement including the coclustering of beta 1 integrins and MT1-matrix metalloproteinase (MMP) at fiber bindings sites and the generation of tube-like proteolytic degradation tracks. Near-total inhibition of MMPs, serine proteases, cathepsins, and other proteases, however, induced a conversion toward spherical morphology at near undiminished migration rates. Sustained protease-independent migration resulted from a flexible amoeba-like shape change, i.e., propulsive squeezing through preexisting matrix gaps and formation of constriction rings in the absence of matrix degradation, concomitant loss of clustered beta 1 integrins and MT1-MMP from fiber binding sites, and a diffuse cortical distribution of the actin cytoskeleton. Acquisition of protease-independent amoeboid dissemination was confirmed for HT-1080 cells injected into the mouse dermis monitored by intravital multiphoton microscopy. In conclusion, the transition from proteolytic mesenchymal toward nonproteolytic amoeboid movement highlights a supramolecular plasticity mechanism in cell migration and further represents a putative escape mechanism in tumor cell dissemination after abrogation of pericellular proteolysis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Actins / metabolism
  • Amoeba / cytology
  • Amoeba / metabolism
  • Animals
  • Cell Movement / physiology*
  • Cell Size / physiology
  • Collagen / metabolism
  • Dermis / cytology
  • Dermis / metabolism
  • Endopeptidases / drug effects
  • Endopeptidases / metabolism
  • Extracellular Matrix Proteins / metabolism*
  • Female
  • Humans
  • Integrin beta1 / metabolism
  • Matrix Metalloproteinase 14
  • Matrix Metalloproteinases, Membrane-Associated
  • Mesoderm / cytology
  • Mesoderm / metabolism*
  • Mesoderm / transplantation
  • Metalloendopeptidases / metabolism
  • Mice
  • Neoplasm Metastasis / physiopathology*
  • Neoplasms / metabolism*
  • Peptide Hydrolases / metabolism
  • Protease Inhibitors / pharmacology
  • Tissue Transplantation
  • Tumor Cells, Cultured

Substances

  • Actins
  • Extracellular Matrix Proteins
  • Integrin beta1
  • Mmp14 protein, mouse
  • Protease Inhibitors
  • Collagen
  • Endopeptidases
  • Peptide Hydrolases
  • Matrix Metalloproteinases, Membrane-Associated
  • Metalloendopeptidases
  • Matrix Metalloproteinase 14