Cancer cell motility: lessons from migration in confined spaces

Time-lapse, deep-tissue imaging made possible by advances in intravital microscopy has demonstrated the importance of tumour cell migration through confining tracks in vivo. These tracks may either be endogenous features of tissues or be created by tumour or tumour-associated cells. Importantly, migration mechanisms through confining microenvironments are not predicted by 2D migration assays. Engineered in vitro models have been used to delineate the mechanisms of cell motility through confining spaces encountered in vivo. Understanding cancer cell locomotion through physiologically relevant confining tracks could be useful in developing therapeutic strategies to combat metastasis.

[1]  G. Charras,et al.  Polar stimulation and constrained cell migration in microfluidic channels. , 2007, Lab on a chip.

[2]  J. Aubertin,et al.  Fine control of nuclear confinement identifies a threshold deformation leading to lamina rupture and induction of specific genes. , 2012, Integrative biology : quantitative biosciences from nano to macro.

[3]  D. Barber,et al.  p160ROCK mediates RhoA activation of Na–H exchange , 1998, The EMBO journal.

[4]  Monika Ritsch-Marte,et al.  Cortical Contractility Triggers a Stochastic Switch to Fast Amoeboid Cell Motility , 2015, Cell.

[5]  J. Joanny,et al.  Physics of active jamming during collective cellular motion in a monolayer , 2015, Proceedings of the National Academy of Sciences.

[6]  Ralph Weissleder,et al.  In vivo molecular target assessment of matrix metalloproteinase inhibition , 2001, Nature Medicine.

[7]  K. Stroka,et al.  Probing cell traction forces in confined microenvironments. , 2013, Lab on a chip.

[8]  P. Friedl,et al.  Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. , 2011, Trends in cell biology.

[9]  Jan Lammerding,et al.  Nuclear Envelope Composition Determines the Ability of Neutrophil-type Cells to Passage through Micron-scale Constrictions* , 2013, The Journal of Biological Chemistry.

[10]  Amber N. Stratman,et al.  MT1-MMP- and Cdc42-dependent signaling co-regulate cell invasion and tunnel formation in 3D collagen matrices , 2009, Journal of Cell Science.

[11]  Anjana Jain,et al.  Guiding intracortical brain tumour cells to an extracortical cytotoxic hydrogel using aligned polymeric nanofibres. , 2014, Nature materials.

[12]  Kevin W Eliceiri,et al.  Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. , 2008, Biophysical journal.

[13]  H. Jeon,et al.  Aquaporin-5: A Marker Protein for Proliferation and Migration of Human Breast Cancer Cells , 2011, PloS one.

[14]  Nicola Elvassore,et al.  Role of YAP/TAZ in mechanotransduction , 2011, Nature.

[15]  Jan Lammerding,et al.  Nuclear envelope rupture and repair during cancer cell migration , 2016, Science.

[16]  Leah Edelstein-Keshet,et al.  Synthetic spatially graded Rac activation drives cell polarization and movement , 2012, Proceedings of the National Academy of Sciences.

[17]  David Erickson,et al.  Elucidating mechanical transition effects of invading cancer cells with a subnucleus-scaled microfluidic serial dimensional modulation device. , 2013, Lab on a chip.

[18]  Lev Truskinovsky,et al.  Volume Changes During Active Shape Fluctuations in Cells. , 2015, Physical review letters.

[19]  Fan-Gang Tseng,et al.  Cell Migration in Microfluidic Devices: Invadosomes Formation in Confined Environments. , 2019, Advances in experimental medicine and biology.

[20]  Andrew J. Ewald,et al.  Matrix metalloproteinases and the regulation of tissue remodelling , 2007, Nature Reviews Molecular Cell Biology.

[21]  K. Stroka,et al.  Distinct signaling mechanisms regulate migration in unconfined versus confined spaces , 2013, The Journal of cell biology.

[22]  Kenneth M. Yamada,et al.  At the leading edge of three-dimensional cell migration , 2012, Journal of Cell Science.

[23]  Stephanie Alexander,et al.  Cancer Invasion and the Microenvironment: Plasticity and Reciprocity , 2011, Cell.

[24]  Anna Haeger,et al.  Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinement. , 2014, Biochimica et biophysica acta.

[25]  Olga Ilina,et al.  Interstitial guidance of cancer invasion , 2012, The Journal of pathology.

[26]  Michael A. Hollingsworth,et al.  Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver , 2015, Nature Cell Biology.

[27]  Pere Roca-Cusachs,et al.  Finding the weakest link – exploring integrin-mediated mechanical molecular pathways , 2012, Journal of Cell Science.

[28]  T. Potapova,et al.  Aneuploidy and chromosomal instability: a vicious cycle driving cellular evolution and cancer genome chaos , 2013, Cancer and Metastasis Reviews.

[29]  Harald Sontheimer,et al.  A neurocentric perspective on glioma invasion , 2014, Nature Reviews Neuroscience.

[30]  Kenneth M. Yamada,et al.  New dimensions in cell migration , 2012, Nature Reviews Molecular Cell Biology.

[31]  Sean X. Sun,et al.  Bioengineering paradigms for cell migration in confined microenvironments. , 2014, Current opinion in cell biology.

[32]  A. Levchenko,et al.  Interplay between chemotaxis and contact inhibition of locomotion determines exploratory cell migration , 2015, Nature Communications.

[33]  C. Moon,et al.  Expression of Aquaporin 5 (AQP5) Promotes Tumor Invasion in Human Non Small Cell Lung Cancer , 2008, PloS one.

[34]  Kenneth M. Yamada,et al.  Fibroblasts Lead the Way: A Unified View of 3D Cell Motility. , 2015, Trends in cell biology.

[35]  Peter Friedl,et al.  Proteolytic interstitial cell migration: a five-step process , 2009, Cancer and Metastasis Reviews.

[36]  Timothy J. Mitchison,et al.  Biased migration of confined neutrophil-like cells in asymmetric hydraulic environments , 2013, Proceedings of the National Academy of Sciences.

[37]  Manuela Schmidt,et al.  Piezo1 and Piezo2 Are Essential Components of Distinct Mechanically Activated Cation Channels , 2010, Science.

[38]  K. Konstantopoulos,et al.  Interplay of the physical microenvironment, contact guidance, and intracellular signaling in cell decision making , 2016, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[39]  H. Parmar,et al.  Epithelial-stromal interactions in the mouse and human mammary gland in vivo. , 2004, Endocrine-related cancer.

[40]  Harihara Baskaran,et al.  A microfluidic imaging chamber for the direct observation of chemotactic transmigration , 2010, Biomedical microdevices.

[41]  Stephen J. Weiss,et al.  Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited , 2009, The Journal of cell biology.

[42]  Shawn P. Carey,et al.  Microfabricated collagen tracks facilitate single cell metastatic invasion in 3D. , 2013, Integrative biology : quantitative biosciences from nano to macro.

[43]  P. Friedl,et al.  Preclinical intravital microscopy of the tumour-stroma interface: invasion, metastasis, and therapy response. , 2013, Current opinion in cell biology.

[44]  Richard Superfine,et al.  Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus , 2014, Nature Cell Biology.

[45]  Marion Ghibaudo,et al.  Hutchinson-Gilford progeria syndrome alters nuclear shape and reduces cell motility in three dimensional model substrates. , 2013, Integrative biology : quantitative biosciences from nano to macro.

[46]  Jacco van Rheenen,et al.  Intravital Microscopy Through an Abdominal Imaging Window Reveals a Pre-Micrometastasis Stage During Liver Metastasis , 2012, Science Translational Medicine.

[47]  M. Nussenzweig,et al.  Dynamic signaling by T follicular helper cells during germinal center B cell selection , 2014, Science.

[48]  P. Steeg,et al.  Targeting metastasis , 2016, Nature Reviews Cancer.

[49]  D. Hartshorne,et al.  Calyculin-A increases the level of protein phosphorylation and changes the shape of 3T3 fibroblasts. , 1991, Cell motility and the cytoskeleton.

[50]  Jacco van Rheenen,et al.  Collagen-based cell migration models in vitro and in vivo. , 2009, Seminars in cell & developmental biology.

[51]  Guillaume Charras,et al.  Physical influences of the extracellular environment on cell migration , 2014, Nature Reviews Molecular Cell Biology.

[52]  Peter Friedl,et al.  Tube travel: the role of proteases in individual and collective cancer cell invasion. , 2008, Cancer research.

[53]  B. Fingleton,et al.  Matrix Metalloproteinase Inhibitors and Cancer—Trials and Tribulations , 2002, Science.

[54]  Matthew J Dalby,et al.  Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. , 2003, Experimental cell research.

[55]  Chwee Teck Lim,et al.  Emerging modes of collective cell migration induced by geometrical constraints , 2012, Proceedings of the National Academy of Sciences.

[56]  M. Piel,et al.  Study of cell migration in microfabricated channels. , 2014, Journal of visualized experiments : JoVE.

[57]  Claudio G. Rolli,et al.  Impact of Tumor Cell Cytoskeleton Organization on Invasiveness and Migration: A Microchannel-Based Approach , 2010, PloS one.

[58]  Mehmet Toner,et al.  Collective and Individual Migration following the Epithelial-Mesenchymal Transition , 2014, Nature materials.

[59]  Rakesh K. Jain,et al.  Pathology: Cancer cells compress intratumour vessels , 2004, Nature.

[60]  D. Di Carlo,et al.  Well-plate mechanical confinement platform for studies of mechanical mutagenesis , 2014, Biomedical microdevices.

[61]  Stephanie Alexander,et al.  Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model , 2008, Histochemistry and Cell Biology.

[62]  I. Fidler,et al.  AACR centennial series: the biology of cancer metastasis: historical perspective. , 2010, Cancer research.

[63]  Elisabeth Wong,et al.  A Worldwide Competition to Compare the Speed and Chemotactic Accuracy of Neutrophil-Like Cells , 2016, PloS one.

[64]  Meng Yang,et al.  Real-time in vivo dual-color imaging of intracapillary cancer cell and nucleus deformation and migration. , 2005, Cancer research.

[65]  P. Friedl,et al.  Intravital third harmonic generation microscopy of collective melanoma cell invasion , 2012, Intravital.

[66]  Gaudenz Danuser,et al.  Myosin-II controls cellular branching morphogenesis and migration in 3D by minimizing cell surface curvature , 2014, Nature Cell Biology.

[67]  M. Sagawa,et al.  Relationship of aquaporin 1, 3, and 5 expression in lung cancer cells to cellular differentiation, invasive growth, and metastasis potential. , 2011, Human pathology.

[68]  K. Stroka,et al.  Physical confinement alters tumor cell adhesion and migration phenotypes , 2012, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[69]  Gaudenz Danuser,et al.  Competition of two distinct actin networks for actin defines a bistable switch for cell polarization , 2015, Nature Cell Biology.

[70]  C. Lugassy,et al.  Angiotropic Melanoma and Extravascular Migratory Metastasis: A Review , 2007, Advances in anatomic pathology.

[71]  Kenneth M. Yamada,et al.  Random versus directionally persistent cell migration , 2009, Nature Reviews Molecular Cell Biology.

[72]  M. Davidson,et al.  RETRACTED: FMN2 Makes Perinuclear Actin to Protect Nuclei during Confined Migration and Promote Metastasis , 2016, Cell.

[73]  Kenneth M. Yamada,et al.  Nonpolarized signaling reveals two distinct modes of 3D cell migration , 2012, The Journal of cell biology.

[74]  F. Nestle,et al.  Diverse matrix metalloproteinase functions regulate cancer amoeboid migration , 2014, Nature Communications.

[75]  J. Segall,et al.  Coordinated regulation of pathways for enhanced cell motility and chemotaxis is conserved in rat and mouse mammary tumors. , 2007, Cancer research.

[76]  H. Pasolli,et al.  Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation , 2011, Nature Cell Biology.

[77]  Andrew Callan-Jones,et al.  Confinement and Low Adhesion Induce Fast Amoeboid Migration of Slow Mesenchymal Cells , 2015, Cell.

[78]  M. Sixt,et al.  Cdc42-dependent leading edge coordination is essential for interstitial dendritic cell migration. , 2009, Blood.

[79]  Pei-Hsun Wu,et al.  Confinement Sensing and Signal Optimization via Piezo1/PKA and Myosin II Pathways , 2016, Cell reports.

[80]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[81]  G. Naumov,et al.  Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis. , 1999, Journal of cell science.

[82]  G. Charras,et al.  Mechanisms of leading edge protrusion in interstitial migration , 2013, Nature Communications.

[83]  Jeffrey Wyckoff,et al.  Invasion of human breast cancer cells in vivo requires both paracrine and autocrine loops involving the colony-stimulating factor-1 receptor. , 2009, Cancer research.

[84]  Sanjay Kumar,et al.  Transforming potential and matrix stiffness co-regulate confinement sensitivity of tumor cell migration. , 2013, Integrative biology : quantitative biosciences from nano to macro.

[85]  L. Szewczak When a Stomach Bug Comes Calling , 2016, Cell.

[86]  M. Davidson,et al.  FMN 2 Makes Perinuclear Actin to Protect Nuclei during Confined Migration and Promote Metastasis , 2016 .

[87]  Olga Ilina,et al.  Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMP-dependent and -independent collective cancer cell invasion , 2011, Physical biology.

[88]  Andrea Dimitracopoulos,et al.  Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation. , 2013, Developmental cell.

[89]  H. Kleinman,et al.  Imaging of Angiotropism/Vascular Co-Option in a Murine Model of Brain Melanoma: Implications for Melanoma Progression along Extravascular Pathways , 2016, Scientific Reports.

[90]  Ravi A. Desai,et al.  Force transmission during adhesion-independent migration , 2015, Nature Cell Biology.

[91]  Erik Sahai,et al.  Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis , 2003, Nature Cell Biology.

[92]  Jean-François Rupprecht,et al.  Actin Flows Mediate a Universal Coupling between Cell Speed and Cell Persistence , 2015, Cell.

[93]  Matthew R. Dallas,et al.  Chemotaxis of Cell Populations through Confined Spaces at Single-Cell Resolution , 2012, PloS one.

[94]  Kenneth M. Yamada,et al.  One-dimensional topography underlies three-dimensional fibrillar cell migration , 2009, The Journal of cell biology.

[95]  Paul A. Bates,et al.  Matrix geometry determines optimal cancer cell migration strategy and modulates response to interventions , 2013, Nature Cell Biology.

[96]  Christopher Beadle,et al.  The role of myosin II in glioma invasion of the brain. , 2008, Molecular biology of the cell.

[97]  Peter Friedl,et al.  Compensation mechanism in tumor cell migration , 2003, The Journal of cell biology.

[98]  Donna J. Webb,et al.  New dimensions in cell migration , 2003, Nature Cell Biology.

[99]  Yu-Li Wang,et al.  Fibroblasts probe substrate rigidity with filopodia extensions before occupying an area , 2014, Proceedings of the National Academy of Sciences.

[100]  Martin Bergert,et al.  Cell mechanics control rapid transitions between blebs and lamellipodia during migration , 2012, Proceedings of the National Academy of Sciences.

[101]  Denis Wirtz,et al.  The physics of cancer: the role of physical interactions and mechanical forces in metastasis , 2011, Nature Reviews Cancer.

[102]  Shawn P. Carey,et al.  Comparative mechanisms of cancer cell migration through 3D matrix and physiological microtracks. , 2015, American journal of physiology. Cell physiology.

[103]  John S. Condeelis,et al.  ROCK- and Myosin-Dependent Matrix Deformation Enables Protease-Independent Tumor-Cell Invasion In Vivo , 2006, Current Biology.

[104]  Ricardo Garcia,et al.  Biomechanical Remodeling of the Microenvironment by Stromal Caveolin-1 Favors Tumor Invasion and Metastasis , 2011, Cell.

[105]  Philipp Niethammer,et al.  The Cell Nucleus Serves as a Mechanotransducer of Tissue Damage-Induced Inflammation , 2016, Cell.

[106]  S. Carmichael,et al.  Angiotropism, Pericytic Mimicry and Extravascular Migratory Metastasis in Melanoma: An Alternative to Intravascular Cancer Dissemination , 2014, Cancer Microenvironment.

[107]  Denis Wirtz,et al.  Engineered Models of Confined Cell Migration. , 2016, Annual review of biomedical engineering.

[108]  J. Lammerding,et al.  Nuclear Deformability Constitutes a Rate-Limiting Step During Cell Migration in 3-D Environments , 2014, Cellular and molecular bioengineering.

[109]  Jochen Herms,et al.  Real-time imaging reveals the single steps of brain metastasis formation , 2010, Nature Medicine.

[110]  P. Friedl,et al.  Interstitial cell migration: integrin-dependent and alternative adhesion mechanisms , 2009, Cell and Tissue Research.

[111]  Sanjay Kumar,et al.  Independent regulation of tumor cell migration by matrix stiffness and confinement , 2012, Proceedings of the National Academy of Sciences.

[112]  K. Konstantopoulos,et al.  Fluid shear promotes chondrosarcoma cell invasion by activating matrix metalloproteinase 12 via IGF-2 and VEGF signaling pathways , 2014, Oncogene.

[113]  Paolo P. Provenzano,et al.  Collagen reorganization at the tumor-stromal interface facilitates local invasion , 2006, BMC medicine.

[114]  Jeffrey Wyckoff,et al.  Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy , 2005, BMC biotechnology.

[115]  Robert S. Adelstein,et al.  Local Cortical Tension by Myosin II Guides 3D Endothelial Cell Branching , 2009, Current Biology.

[116]  J. Massagué,et al.  Cancer Metastasis: Building a Framework , 2006, Cell.

[117]  Erez Raz,et al.  The role and regulation of blebs in cell migration , 2013, Current opinion in cell biology.

[118]  R. Voituriez,et al.  ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death , 2016, Science.

[119]  M. Clarke,et al.  Intravital multiphoton imaging reveals multicellular streaming as a crucial component of in vivo cell migration in human breast tumors , 2013, Intravital.

[120]  M. Clarke,et al.  Reconstitution of in vivo macrophage-tumor cell pairing and streaming motility on one-dimensional micro-patterned substrates , 2012, Intravital.

[121]  Dino Di Carlo,et al.  Increased Asymmetric and Multi-Daughter Cell Division in Mechanically Confined Microenvironments , 2012, PloS one.

[122]  B. R. Bass,et al.  3D collagen alignment limits protrusions to enhance breast cancer cell persistence. , 2014, Biophysical journal.

[123]  D. Barber,et al.  p 160 ROCK mediates RhoA activation of Na – H exchange , 2013 .

[124]  Stephen Pulman,et al.  Building the Framework , 1996 .

[125]  Paolo P. Provenzano,et al.  Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma Address Reprint Requests to See Related Commentary on Page 966 , 2022 .

[126]  Kevin E. Healy,et al.  Engineering gene expression and protein synthesis by modulation of nuclear shape , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[127]  J. Joanny,et al.  Pushing off the walls: a mechanism of cell motility in confinement. , 2009, Physical review letters.

[128]  L. Qin,et al.  Utilizing a high-throughput microfluidic platform to study hypoxia-driven mesenchymal-mode cell migration. , 2015, Integrative biology : quantitative biosciences from nano to macro.

[129]  Robert M. Hoffman,et al.  Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force , 2013, The Journal of cell biology.

[130]  E. Sahai,et al.  Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells , 2007, Nature Cell Biology.

[131]  M. Stack,et al.  Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion , 2007, Nature Cell Biology.

[132]  K. Stroka,et al.  Physical biology in cancer. 4. Physical cues guide tumor cell adhesion and migration. , 2014, American journal of physiology. Cell physiology.

[133]  Paul A. Bates,et al.  STRIPAK components determine mode of cancer cell migration and metastasis , 2014, Nature Cell Biology.

[134]  S. Hanks,et al.  Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. , 2006, Biophysical journal.

[135]  Denis Wirtz,et al.  Water Permeation Drives Tumor Cell Migration in Confined Microenvironments , 2014, Cell.

[136]  Mehmet Toner,et al.  Epithelial cell guidance by self-generated EGF gradients. , 2012, Integrative biology : quantitative biosciences from nano to macro.