One-dimensional topography underlies three-dimensional fibrillar cell migration

By A. Doyle, Francis W. Wang, Kazue Matsumoto, Kenneth M. Yamada. Journal of Cell Biology, 2009

748 citations recorded by the source corpus.

Current concepts of cell migration were established in regular two-dimensional (2D) cell culture, but the roles of topography are poorly understood for cells migrating in an oriented 3D fibrillar extracellular matrix (ECM). We use a novel micropatterning technique termed microphotopatterning (μPP) to identify functions for 1D fibrillar patterns in 3D cell migration. In striking contrast to 2D, cell migration in both 1D and 3D is rapid, uniaxial, independent of ECM ligand density, and dependent on myosin II contractility and microtubules (MTs). 1D and 3D migration are also characterized by an anterior MT bundle with a posterior centrosome. We propose that cells migrate rapidly through 3D fibrillar matrices by a 1D migratory mechanism not mimicked by 2D matrices.

Subfields: Biomedical Engineering, Cell Biology, Immunology and Allergy

View Paper: https://www.semanticscholar.org/paper/78ddb2f8b914374ef94135f1b152216740504d72

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Citations in the corpus

Random versus directionally persistent cell migration (2009, background): “Cell migration along a highly oriented matrix is directional and rapi”
Biomechanical remodeling of the microenvironment by stromal Caveolin-1 favors tumor invasion and metastasis (2011, background): “Contact guidance implies that structural organization of ECM provides directional cues to cells and directs morphology and motility via anisotropy of the microenvironment (Doyle et al., 2009).”
Engineering microscale topographies to control the cell–substrate interface (2012, methodology): “Microfabricated substrates with asymmetric topographies have been used to recapitulate the directional migration of cells mediated by ECM topography.”
The Extracellular Matrix In Development and Morphogenesis: A Dynamic View (2009, background): “…consequences of assembly state to specific developmental events in vivo, a number of cell culture experiments in recent years serve to highlight the importance of “matrix-topography” to cell physiology (Cukierman et al., 2001; Mao and Schwarzbauer, 2005) andmigration (Doyle et al., 2009).”
Micropatterning as a tool to decipher cell morphogenesis and functions (2010, background): “…than those grown on a homogeneous substrate surface and display most of the characteristics of cells that migrate in collagen gels; i.e. a coordinated displacement of cell front and cell body, and dependency on acto-myosin contractility and microtubules (Doyle et al., 2009; Pouthas et al., 2008).”
Cell adhesion: integrating cytoskeletal dynamics and cellular tension (2010, background): “The adhesions of cells attached to large collagen fibres are large and oriented along the fibres in a two-dimensional (2D)-like organizatio”
Actin dynamics, architecture, and mechanics in cell motility. (2014, background): “It should be pointed out that with the advent of culture conditions that more closely mimic the in vivo environment (3-dimensional geometries with adjustable mechanical properties), as well as developments in in vivo imaging of cell motility, it is becoming increasingly apparent that not all migrati”
Balancing forces: architectural control of mechanotransduction (2011, neutral): “For instance, cells cultured in 1D, 2D and 3D show pronounced differences in their motilit”
Integrins in cell migration. (2011, neutral): “2005, 2006, 2007) but not for others (Doyle et al. 2009).”
Deconstructing the third dimension – how 3D culture microenvironments alter cellular cues (2012, methodology): “Images in the Figure were adapted with permission from Grinnell et al., 2003 (A), Doyle et al., 2009 (C) and Legant et al., 2010 (D) (Grinnell et al., 2003; Doyle et al., 2009; Legant et al., 2010).”
Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells (2009, background): “demonstrate the role played by topography in the migration of fibroblasts on a one-dimensional fibrillar pattern and three-dimensional matrix [6].”