Influence of the microenvironment on cell fate determination and migration.

Several critical cell functions are influenced not only by internal cellular machinery but also by external mechanical and biochemical cues from the surrounding microenvironment. Slight changes to the microenvironment can result in dramatic changes to the cell's phenotype; for example, a change in the nutrients or pH of a tumor microenvironment can result in increased tumor metastasis. While cellular fate and the regulators of cell fate have been studied in detail for several decades now, our understanding of the extracellular regulators remains qualitative and far from comprehensive. In this review, we discuss the microenvironment influence on cell fate in terms of adhesion, migration, and differentiation and focus on both developments in experimental and computation tools to analyze cellular fate.

[1]  Sunitha Nagrath,et al.  Microfluidics and cancer: are we there yet? , 2013, Biomedical microdevices.

[2]  J. Guan,et al.  Analysis of directional cell migration on defined FN gradients: role of intracellular signaling molecules. , 2007, Experimental cell research.

[3]  JONG BIN Kim,et al.  Three-dimensional tissue culture models in cancer biology. , 2005, Seminars in cancer biology.

[4]  A. Levchenko,et al.  Lab-on-a-chip devices as an emerging platform for stem cell biology. , 2010, Lab on a chip.

[5]  Dewi Harjanto,et al.  Matrix mechanics and receptor-ligand interactions in cell adhesion. , 2010, Organic & biomolecular chemistry.

[6]  Muhammad H Zaman,et al.  Modeling cell migration in 3D , 2008, Cell adhesion & migration.

[7]  Raghu Kalluri,et al.  The basics of epithelial-mesenchymal transition. , 2009, The Journal of clinical investigation.

[8]  Manuel Théry,et al.  A new micropatterning method of soft substrates reveals that different tumorigenic signals can promote or reduce cell contraction levels. , 2011, Lab on a chip.

[9]  Sirio Dupont.  Role of YAP/TAZ in mechanotransduction , 2011 .

[10]  R. Vatsyayan,et al.  The sensors and regulators of cell–matrix surveillance in anoikis resistance of tumors , 2011, International journal of cancer.

[11]  Tiffany W Guo,et al.  Epidermal growth factor-induced enhancement of glioblastoma cell migration in 3D arises from an intrinsic increase in speed but an extrinsic matrix- and proteolysis-dependent increase in persistence. , 2008, Molecular biology of the cell.

[12]  M. Mareel,et al.  Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. , 2001, Journal of cell science.

[13]  Roger D Kamm,et al.  Microfluidic platforms for mechanobiology. , 2013, Lab on a chip.

[14]  R. Sandberg,et al.  Gene expression perturbation in vitro--a growing case for three-dimensional (3D) culture systems. , 2005, Seminars in cancer biology.

[15]  T. Alliston,et al.  ECM stiffness primes the TGFβ pathway to promote chondrocyte differentiation , 2012, Molecular biology of the cell.

[16]  S. Thrun,et al.  Substrate Elasticity Regulates Skeletal Muscle Stem Cell Self-Renewal in Culture , 2010, Science.

[17]  Yang Jiao,et al.  Emergent Behaviors from a Cellular Automaton Model for Invasive Tumor Growth in Heterogeneous Microenvironments , 2011, PLoS Comput. Biol..

[18]  E. Brandan,et al.  ECM is required for skeletal muscle differentiation independently of muscle regulatory factor expression. , 2002, American journal of physiology. Cell physiology.

[19]  Song Li,et al.  Regulation of the Matrix Microenvironment for Stem Cell Engineering and Regenerative Medicine , 2011, Annals of Biomedical Engineering.

[20]  N. Boudreau,et al.  Extracellular matrix and integrin signalling: the shape of things to come. , 1999, The Biochemical journal.

[21]  Kshitiz,et al.  Control of stem cell fate and function by engineering physical microenvironments. , 2012, Integrative biology : quantitative biosciences from nano to macro.

[22]  Sergey V. Plotnikov,et al.  Force Fluctuations within Focal Adhesions Mediate ECM-Rigidity Sensing to Guide Directed Cell Migration , 2012, Cell.

[23]  Farshid Guilak,et al.  Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. , 2010, Biomaterials.

[24]  Shawn M. Sweeney,et al.  Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen* , 2002, The Journal of Biological Chemistry.

[25]  Yi-Chun Wu,et al.  Engulfment of Apoptotic Cells in C. elegans Is Mediated by Integrin α/SRC Signaling , 2010, Current Biology.

[26]  L. Griffith,et al.  Capturing complex 3D tissue physiology in vitro , 2006, Nature Reviews Molecular Cell Biology.

[27]  D. Lauffenburger,et al.  A high-throughput migration assay reveals HER2-mediated cell migration arising from increased directional persistence. , 2006, Biophysical journal.

[28]  R. Brown,et al.  Interface integration of layered collagen scaffolds with defined matrix stiffness: implications for sheet‐based tissue engineering , 2009, Journal of tissue engineering and regenerative medicine.

[29]  Kuo-Kang Liu,et al.  Biomimetic three-dimensional microenvironment for controlling stem cell fate , 2011, Interface Focus.

[30]  D. Lauffenburger,et al.  Measurement and modeling of signaling at the single-cell level. , 2012, Biochemistry.

[31]  Kenneth M. Yamada,et al.  Taking Cell-Matrix Adhesions to the Third Dimension , 2001, Science.

[32]  F. Aoudjit,et al.  Integrin signaling inhibits paclitaxel-induced apoptosis in breast cancer cells , 2001, Oncogene.

[33]  David J. Mooney,et al.  Harnessing Traction-Mediated Manipulation of the Cell-Matrix Interface to Control Stem Cell Fate , 2010, Nature materials.

[34]  Peter T. Cummings,et al.  An off-lattice hybrid discrete-continuum model of tumor growth and invasion. , 2010, Biophysical journal.

[35]  Mauro Ferrari,et al.  Multiparameter computational modeling of tumor invasion. , 2009, Cancer research.

[36]  Peng-Yuan Wang,et al.  Screening of rat mesenchymal stem cell behaviour on polydimethylsiloxane stiffness gradients. , 2012, Acta biomaterialia.

[37]  B. Thiers.  Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors , 2008 .

[38]  Shoham Shivtiel,et al.  Stem cell regulation via dynamic interactions of the nervous and immune systems with the microenvironment. , 2008, Cell stem cell.

[39]  Seung-Yoon Park,et al.  Cross Talk between Engulfment Receptors Stabilin-2 and Integrin αvβ5 Orchestrates Engulfment of Phosphatidylserine-Exposed Erythrocytes , 2012, Molecular and Cellular Biology.

[40]  G. Schultz,et al.  Interactions between extracellular matrix and growth factors in wound healing , 2009, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[41]  David A. Cheresh,et al.  Get a ligand, get a life: integrins, signaling and cell survival , 2002, Journal of Cell Science.

[42]  Stephanie I. Fraley,et al.  A distinctive role for focal adhesion proteins in three-dimensional cell motility , 2010, Nature Cell Biology.

[43]  J. Foidart,et al.  Upregulation of MMPs by soluble E‐cadherin in human lung tumor cells , 2003, International journal of cancer.

[44]  Albert J. Keung,et al.  Substrate modulus directs neural stem cell behavior. , 2008, Biophysical journal.

[45]  F. Omenetto,et al.  Bio‐microfluidics: Biomaterials and Biomimetic Designs , 2010, Advanced materials.

[46]  Min Sung Kim,et al.  Nanotopography-guided tissue engineering and regenerative medicine. , 2013, Advanced drug delivery reviews.

[47]  Andre Levchenko,et al.  Matrix nanotopography as a regulator of cell function , 2012, The Journal of cell biology.

[48]  Donald E Ingber,et al.  Mechanobiology and developmental control. , 2013, Annual review of cell and developmental biology.

[49]  Robin A Felder,et al.  3D cell culture opens new dimensions in cell-based assays. , 2009, Drug discovery today.

[50]  Yong‐Nyun Kim,et al.  Anoikis Resistance: An Essential Prerequisite for Tumor Metastasis , 2012, International journal of cell biology.

[51]  Shangxin Liu,et al.  Integrin β1 is required for dermal homeostasis. , 2013, The Journal of investigative dermatology.

[52]  Fiona M. Watt,et al.  Role of the extracellular matrix in regulating stem cell fate , 2013, Nature Reviews Molecular Cell Biology.

[53]  Brendon M. Baker,et al.  Deconstructing the third dimension – how 3D culture microenvironments alter cellular cues , 2012, Journal of Cell Science.

[54]  Mark A. J. Chaplain,et al.  Mathematical modeling of cancer cell invasion of tissue: biological insight from mathematical analysis and computational simulation , 2011, Journal of mathematical biology.

[55]  W. Kisaalita,et al.  Biomarkers for simplifying HTS 3D cell culture platforms for drug discovery: the case for cytokines. , 2011, Drug discovery today.

[56]  G. Christofori.  New signals from the invasive front , 2006, Nature.

[57]  S. Yamanaka,et al.  Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors , 2006, Cell.

[58]  Choon Kiat Lim,et al.  Nanotopography modulates mechanotransduction of stem cells and induces differentiation through focal adhesion kinase. , 2013, ACS nano.

[59]  A. Anderson,et al.  A hybrid mathematical model of solid tumour invasion: the importance of cell adhesion , 2005 .

[60]  J. Delord,et al.  Implication of Tumor Microenvironment in Chemoresistance: Tumor-Associated Stromal Cells Protect Tumor Cells from Cell Death , 2012, International journal of molecular sciences.

[61]  H. Harry Asada,et al.  Dynamic Modeling of Cell Migration and Spreading Behaviors on Fibronectin Coated Planar Substrates and Micropatterned Geometries , 2013, PLoS Comput. Biol..

[62]  K. Smalley,et al.  Fibroblast-mediated drug resistance in cancer. , 2013, Biochemical pharmacology.

[63]  E. Golemis,et al.  Fibroblast-derived 3D matrix differentially regulates the growth and drug-responsiveness of human cancer cells. , 2008, Matrix biology : journal of the International Society for Matrix Biology.

[64]  H. Bégueret,et al.  Three-dimensional culture model to distinguish normal from malignant human bronchial epithelial cells , 2013, European Respiratory Journal.

[65]  Z. Werb,et al.  ECM signalling: orchestrating cell behaviour and misbehaviour. , 1998, Trends in cell biology.

[66]  S. Sen,et al.  Matrix Elasticity Directs Stem Cell Lineage Specification , 2006, Cell.

[67]  Dewi Harjanto,et al.  Computational Study of Proteolysis-Driven Single Cell Migration in a Three-Dimensional Matrix , 2010, Annals of Biomedical Engineering.

[68]  Matthias P Lutolf,et al.  Biomaterials meet microfluidics: building the next generation of artificial niches. , 2011, Current opinion in biotechnology.

[69]  S. Dangi‐Garimella,et al.  Three-dimensional collagen I promotes gemcitabine resistance in pancreatic cancer through MT1-MMP-mediated expression of HMGA2. , 2011, Cancer research.

[70]  Alissa M. Weaver,et al.  Tumor Morphology and Phenotypic Evolution Driven by Selective Pressure from the Microenvironment , 2006, Cell.

[71]  Quan Long,et al.  Coupled modelling of tumour angiogenesis, tumour growth and blood perfusion. , 2011, Journal of theoretical biology.

[72]  A. Shiratsuchi,et al.  Phosphatidylserine‐ and integrin‐mediated phagocytosis of apoptotic luteal cells by macrophages of the rat , 2005, Development, growth & differentiation.

[73]  M. Chalfie,et al.  Eukaryotic mechanosensitive channels. , 2010, Annual review of biophysics.

[74]  Robert J Gillies,et al.  Acidity generated by the tumor microenvironment drives local invasion. , 2013, Cancer research.

[75]  Donald E. Ingber,et al.  A mechanosensitive transcriptional mechanism that controls angiogenesis , 2009, Nature.

[76]  Kshitiz,et al.  Micro- and nanoengineering for stem cell biology: the promise with a caution. , 2011, Trends in biotechnology.

[77]  Peter W. Zandstra,et al.  Towards predictive models of stem cell fate , 2003, Cytotechnology.

[78]  Kshitiz,et al.  Matrix Rigidity Controls Endothelial Differentiation and Morphogenesis of Cardiac Precursors , 2012, Science Signaling.

[79]  John A. Pedersen,et al.  Mechanobiology in the Third Dimension , 2005, Annals of Biomedical Engineering.

[80]  Sha Jin,et al.  Mechanobiology of human pluripotent stem cells. , 2013, Tissue engineering. Part B, Reviews.