Engineering Cell Instructive Materials To Control Cell Fate and Functions through Material Cues and Surface Patterning.

Mastering the interaction between cells and extracellular environment is a fundamental prerequisite in order to engineer functional biomaterial interfaces able to instruct cells with specific commands. Such advanced biomaterials might find relevant application in prosthesis design, tissue engineering, diagnostics and stem cell biology. Because of the highly complex, dynamic, and multifaceted context, a thorough understanding of the cell-material crosstalk has not been achieved yet; however, a variety of material features including biological cues, topography, and mechanical properties have been proved to impact the strength and the nature of the cell-material interaction, eventually affecting cell fate and functions. Although the nature of these three signals may appear very different, they are equated by their participation in the same material-cytoskeleton crosstalk pathway as they regulate cell adhesion events. In this work we present recent and relevant findings on the material-induced cell responses, with a particular emphasis on how the presentation of biochemical/biophysical signals modulates cell behavior. Finally, we summarize and discuss the literature data to draw out unifying elements concerning cell recognition of and reaction to signals displayed by material surfaces.

[1]  J. Hubbell,et al.  An RGD spacing of 440 nm is sufficient for integrin alpha V beta 3- mediated fibroblast spreading and 140 nm for focal contact and stress fiber formation , 1991, The Journal of cell biology.

[2]  Cynthia A. Reinhart-King,et al.  Matrix Stiffness: A Regulator of Cellular Behavior and Tissue Formation , 2012 .

[3]  J. Spatz,et al.  Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. , 2009, Acta biomaterialia.

[4]  A. Harris,et al.  Silicone rubber substrata: a new wrinkle in the study of cell locomotion. , 1980, Science.

[5]  Paolo A Netti,et al.  Determinants of cell–material crosstalk at the interface: towards engineering of cell instructive materials , 2012, Journal of The Royal Society Interface.

[6]  Murat Guvendiren,et al.  Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics , 2012, Nature Communications.

[7]  Joseph Hemmerlé,et al.  Biomimetic cryptic site surfaces for reversible chemo- and cyto-mechanoresponsive substrates. , 2013, ACS nano.

[8]  Jiandong Ding,et al.  Effect of cell anisotropy on differentiation of stem cells on micropatterned surfaces through the controlled single cell adhesion. , 2011, Biomaterials.

[9]  Paolo A Netti,et al.  Crosstalk between focal adhesions and material mechanical properties governs cell mechanics and functions. , 2015, Acta biomaterialia.

[10]  Andre Levchenko,et al.  Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs , 2009, Proceedings of the National Academy of Sciences.

[11]  J. Spatz,et al.  Block Copolymer Micelle Nanolithography , 2003 .

[12]  D. Ingber,et al.  Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus , 2009, Nature Reviews Molecular Cell Biology.

[13]  M. Textor,et al.  Surface engineering approaches to micropattern surfaces for cell-based assays. , 2006, Biomaterials.

[14]  J. Jansen,et al.  The influence of nanoscale topographical cues on initial osteoblast morphology and migration. , 2010, European cells & materials.

[15]  Kshitiz Gupta,et al.  Mechanosensitivity of fibroblast cell shape and movement to anisotropic substratum topography gradients. , 2009, Biomaterials.

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

[17]  Sungho Jin,et al.  Stem cell fate dictated solely by altered nanotube dimension , 2009, Proceedings of the National Academy of Sciences.

[18]  F. Tang,et al.  Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. , 2008, Cell stem cell.

[19]  Nikolaj Gadegaard,et al.  Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. , 2014, Nature materials.

[20]  R. G. Richards,et al.  Nanotopographical modification: a regulator of cellular function through focal adhesions. , 2010, Nanomedicine : nanotechnology, biology, and medicine.

[21]  B. Geiger,et al.  Regulation of Integrin Adhesions by Varying the Density of Substrate-Bound Epidermal Growth Factor , 2012, Biointerphases.

[22]  A. Borzacchiello,et al.  Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters. , 2010, Acta biomaterialia.

[23]  Ning Wang,et al.  Soft Substrates Promote Homogeneous Self-Renewal of Embryonic Stem Cells via Downregulating Cell-Matrix Tractions , 2010, PloS one.

[24]  Jiandong Ding,et al.  Effects of aspect ratios of stem cells on lineage commitments with and without induction media. , 2013, Biomaterials.

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

[26]  Pietro Ferraro,et al.  Reversible Holographic Patterns on Azopolymers for Guiding Cell Adhesion and Orientation. , 2015, ACS applied materials & interfaces.

[27]  Martin A. Schwartz,et al.  Cell adhesion: integrating cytoskeletal dynamics and cellular tension , 2010, Nature Reviews Molecular Cell Biology.

[28]  Daniela Guarnieri,et al.  Surface investigation on biomimetic materials to control cell adhesion: the case of RGD conjugation on PCL. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[29]  Donald E Ingber,et al.  Mechanical control of tissue and organ development , 2010, Development.

[30]  Teodor Veres,et al.  Surface topography induces 3D self-orientation of cells and extracellular matrix resulting in improved tissue function. , 2009, Integrative biology : quantitative biosciences from nano to macro.

[31]  Shelly R. Peyton,et al.  Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion , 2005, Journal of cellular physiology.

[32]  Wesley R. Legant,et al.  Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels , 2013, Nature materials.

[33]  Horst Kessler,et al.  RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. , 2003, Biomaterials.

[34]  Jennifer S. Park,et al.  The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-β. , 2011, Biomaterials.

[35]  Paolo A Netti,et al.  Tuning the material-cytoskeleton crosstalk via nanoconfinement of focal adhesions. , 2014, Biomaterials.

[36]  R. Langer,et al.  Engineering substrate topography at the micro- and nanoscale to control cell function. , 2009, Angewandte Chemie.

[37]  Shelly R. Peyton,et al.  The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells. , 2006, Biomaterials.

[38]  E. Danen,et al.  A guide to mechanobiology: Where biology and physics meet. , 2015, Biochimica et biophysica acta.

[39]  J. Hubbell,et al.  Human endothelial cell interactions with surface-coupled adhesion peptides on a nonadhesive glass substrate and two polymeric biomaterials. , 1991, Journal of biomedical materials research.

[40]  M. Eiraku,et al.  Self-organizing optic-cup morphogenesis in three-dimensional culture , 2011, Neuroscience Research.

[41]  Kam W Leong,et al.  Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. , 2007, Experimental cell research.

[42]  D. Scharnweber,et al.  Functionalization of biomaterial surfaces using artificial extracellular matrices , 2012, Biomatter.

[43]  Joachim P Spatz,et al.  Activation of integrin function by nanopatterned adhesive interfaces. , 2004, Chemphyschem : a European journal of chemical physics and physical chemistry.

[44]  Christopher S. Chen,et al.  Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. , 2004, Developmental cell.

[45]  Milan Mrksich,et al.  Geometric cues for directing the differentiation of mesenchymal stem cells , 2010, Proceedings of the National Academy of Sciences.

[46]  Maurizio Ventre,et al.  Topographic cell instructive patterns to control cell adhesion, polarization and migration , 2014, Journal of The Royal Society Interface.

[47]  Benjamin Geiger,et al.  Molecular architecture and function of matrix adhesions. , 2011, Cold Spring Harbor perspectives in biology.

[48]  John K. Tomfohr,et al.  Measurement of cell migration on surface-bound fibronectin gradients. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[49]  C. S. Chen,et al.  Geometric control of cell life and death. , 1997, Science.

[50]  P. Netti,et al.  Ligand engagement on material surfaces is discriminated by cell mechanosensoring. , 2015, Biomaterials.

[51]  L G Griffith,et al.  Cell adhesion and motility depend on nanoscale RGD clustering. , 2000, Journal of cell science.

[52]  Mikhail Zhernenkov,et al.  Thermoresponsive PNIPAM Coatings on Nanostructured Gratings for Cell Alignment and Release. , 2015, ACS applied materials & interfaces.

[53]  Huaping Tan,et al.  Gradient biomaterials and their influences on cell migration , 2012, Interface Focus.

[54]  Michael P. Sheetz,et al.  Stretching Single Talin Rod Molecules Activates Vinculin Binding , 2009, Science.

[55]  N. Gadegaard,et al.  Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. , 2011, Nature materials.

[56]  T. Munro,et al.  Nanoscale presentation of cell adhesive molecules via block copolymer self-assembly. , 2009, Biomaterials.

[57]  Justin Cooper-White,et al.  The influence of substrate creep on mesenchymal stem cell behaviour and phenotype. , 2011, Biomaterials.

[58]  Michael W. Davidson,et al.  Nanoscale architecture of integrin-based cell adhesions , 2010, Nature.

[59]  Xu,et al.  "Dip-Pen" nanolithography , 1999, Science.

[60]  M. Bissell,et al.  Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. , 2006, Annual review of cell and developmental biology.

[61]  Li Yang,et al.  Biophysical regulation of histone acetylation in mesenchymal stem cells. , 2011, Biophysical journal.

[62]  Mark Schvartzman,et al.  Nanolithographic control of the spatial organization of cellular adhesion receptors at the single-molecule level. , 2011, Nano letters.

[63]  C. Wilkinson,et al.  The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. , 2007, Nature materials.

[64]  Paolo A Netti,et al.  Nanoengineered surfaces for focal adhesion guidance trigger mesenchymal stem cell self-organization and tenogenesis. , 2015, Nano letters.

[65]  Keesung Kim,et al.  Direct differentiation of human embryonic stem cells into selective neurons on nanoscale ridge/groove pattern arrays. , 2010, Biomaterials.

[66]  Gordana Vunjak-Novakovic,et al.  The effect of actin disrupting agents on contact guidance of human embryonic stem cells. , 2007, Biomaterials.

[67]  K. Christman,et al.  Nanoscale growth factor patterns by immobilization on a heparin-mimicking polymer. , 2008, Journal of the American Chemical Society.

[68]  P. Janmey,et al.  Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. , 2005, Cell motility and the cytoskeleton.

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

[70]  Filippo Stefanoni,et al.  Molding Micropatterns of Elasticity on PEG‐Based Hydrogels to Control Cell Adhesion and Migration , 2011 .

[71]  J. Jansen,et al.  The threshold at which substrate nanogroove dimensions may influence fibroblast alignment and adhesion. , 2007, Biomaterials.

[72]  L. Trusolino,et al.  Interactions between growth factor receptors and adhesion molecules: breaking the rules. , 2003, Current opinion in cell biology.

[73]  Sujata K. Bhatia,et al.  Engineering Biomaterials for Regenerative Medicine: Novel Technologies for Clinical Applications , 2012 .

[74]  Juergen A. Knoblich,et al.  Organogenesis in a dish: Modeling development and disease using organoid technologies , 2014, Science.

[75]  Jeffrey R Capadona,et al.  Polymer brushes and self-assembled monolayers: Versatile platforms to control cell adhesion to biomaterials (Review) , 2009, Biointerphases.