From nano to micro: topographical scale and its impact on cell adhesion, morphology and contact guidance

Topography, among other physical factors such as substrate stiffness and extracellular forces, is known to have a great influence on cell behaviours. Optimization of topographical features, in particular topographical dimensions ranging from nanoscale to microscale, is the key strategy to obtain the best cellular performance for various applications in tissue engineering and regenerative medicine. In this review, we provide a comprehensive survey on the significance of sizes of topography and their impacts on cell adhesion, morphology and alignment, and neurite guidance. Also recent works mimicking the hierarchical structure of natural extracellular matrix by combining both nanoscale and microscale topographies are highlighted.

[1]  S. B. Kater,et al.  A sensory role for neuronal growth cone filopodia , 1993, Nature.

[2]  C. Chen,et al.  Membranes of epitaxial-like packed, super aligned electrospun micron hollow poly(l-lactic acid) (PLLA) fibers , 2011 .

[3]  G. Banker,et al.  Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones , 1988, Nature.

[4]  R. Williams,et al.  Growth cones, dying axons, and developmental fluctuations in the fiber population of the cat's optic nerve , 1986, The Journal of comparative neurology.

[5]  J. Jansen,et al.  The influence of nanoscale grooved substrates on osteoblast behavior and extracellular matrix deposition. , 2010, Biomaterials.

[6]  Hanjun Wang,et al.  Varying the diameter of aligned electrospun fibers alters neurite outgrowth and Schwann cell migration. , 2010, Acta biomaterialia.

[7]  K. Chiam,et al.  Extending neurites sense the depth of the underlying topography during neuronal differentiation and contact guidance. , 2014, Biomaterials.

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

[9]  Thomas J Webster,et al.  Improved endothelial cell adhesion and proliferation on patterned titanium surfaces with rationally designed, micrometer to nanometer features. , 2008, Acta biomaterialia.

[10]  S. Britland,et al.  Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. , 1997, Journal of cell science.

[11]  Dario Pisignano,et al.  Combined nano- and micro-scale topographic cues for engineered vascular constructs by electrospinning and imprinted micro-patterns. , 2014, Small.

[12]  S. Ramakrishna,et al.  Electrospinning of nano/micro scale poly(L-lactic acid) aligned fibers and their potential in neural tissue engineering. , 2005, Biomaterials.

[13]  Saida P. Khan,et al.  A comprehensive review of surface modification for neural cell adhesion and patterning. , 2010, Journal of biomedical materials research. Part A.

[14]  Younan Xia,et al.  The differentiation of embryonic stem cells seeded on electrospun nanofibers into neural lineages. , 2009, Biomaterials.

[15]  Christopher J Murphy,et al.  Sub-micron and nanoscale feature depth modulates alignment of stromal fibroblasts and corneal epithelial cells in serum-rich and serum-free media. , 2008, Journal of biomedical materials research. Part A.

[16]  T. Webster,et al.  Increased endothelial and vascular smooth muscle cell adhesion on nanostructured titanium and CoCrMo , 2006, International journal of nanomedicine.

[17]  C. Chen,et al.  Permeation of biological compounds through porous poly(l-lactic acid) (PLLA) microtube array membranes (MTAMs) , 2015 .

[18]  Evelyn K F Yim,et al.  Nanotopography/mechanical induction of stem-cell differentiation. , 2010, Methods in cell biology.

[19]  Lars Montelius,et al.  Axonal outgrowth on nano-imprinted patterns. , 2006, Biomaterials.

[20]  E. Dent,et al.  Cytoskeletal Dynamics and Transport in Growth Cone Motility and Axon Guidance , 2003, Neuron.

[21]  Darrell H. Reneker,et al.  Electrospinning process and applications of electrospun fibers , 1995 .

[22]  P. Weiss In vitro experiments on the factors determining the course of the outgrowing nerve fiber , 1934 .

[23]  D. H. Taylor,et al.  Orientation of Amphibians by Linearly Polarized Light , 1978 .

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

[25]  E. Drioli,et al.  Neuronal growth and differentiation on biodegradable membranes , 2015, Journal of tissue engineering and regenerative medicine.

[26]  R. Buxbaum,et al.  Measurements of growth cone adhesion to culture surfaces by micromanipulation , 1994, The Journal of cell biology.

[27]  J. Brocard,et al.  Nanoscale surface topography reshapes neuronal growth in culture. , 2014, Langmuir : the ACS journal of surfaces and colloids.

[28]  Costas P. Grigoropoulos,et al.  Directing cell migration and organization via nanocrater-patterned cell-repellent interfaces , 2015, Nature materials.

[29]  V. Caracciolo,et al.  Transient maintenance in bioreactor improves health of neuronal cells , 2006, In Vitro Cellular & Developmental Biology - Animal.

[30]  Casey K. Chan,et al.  Synergistic effects of electrospun PLLA fiber dimension and pattern on neonatal mouse cerebellum C17.2 stem cells. , 2010, Acta biomaterialia.

[31]  B. Zuo,et al.  Electrospun silk fibroin nanofibers in different diameters support neurite outgrowth and promote astrocyte migration. , 2013, Journal of biomedical materials research. Part A.

[32]  Bryan J. Pfister,et al.  Axon Stretch Growth: The Mechanotransduction of Neuronal Growth , 2011, Journal of visualized experiments : JoVE.

[33]  P. Saini,et al.  Poly(lactic acid) blends in biomedical applications. , 2016, Advanced drug delivery reviews.

[34]  Enrico Drioli,et al.  Influence of micro-patterned PLLA membranes on outgrowth and orientation of hippocampal neurites. , 2010, Biomaterials.

[35]  L. Dahlin,et al.  Chitosan-film enhanced chitosan nerve guides for long-distance regeneration of peripheral nerves. , 2016, Biomaterials.

[36]  S. Goh,et al.  Enhanced differentiation of neural progenitor cells into neurons of the mesencephalic dopaminergic subtype on topographical patterns. , 2015, Biomaterials.

[37]  H. Low,et al.  Planar and tubular patterning of micro and nano-topographies on poly(vinyl alcohol) hydrogel for improved endothelial cell responses. , 2016, Biomaterials.

[38]  A. Glezer,et al.  Microfluidic engineered high cell density three-dimensional neural cultures , 2007, Journal of neural engineering.

[39]  Kisuk Yang,et al.  Multiscale, hierarchically patterned topography for directing human neural stem cells into functional neurons. , 2014, ACS nano.

[40]  E. Drioli,et al.  Neuronal membrane bioreactor as a tool for testing crocin neuroprotective effect in Alzheimer’s disease , 2016 .

[41]  Keng-Hwee Chiam,et al.  Anisotropic rigidity sensing on grating topography directs human mesenchymal stem cell elongation , 2013, Biomechanics and Modeling in Mechanobiology.

[42]  D. Kaplan,et al.  Induction of TrkB by retinoic acid mediates biologic responsiveness to BDNF and differentiation of human neuroblastoma cells , 1993, Neuron.

[43]  Farshid Guilak,et al.  Micro-scale and meso-scale architectural cues cooperate and compete to direct aligned tissue formation. , 2014, Biomaterials.

[44]  Tong Lin,et al.  Nerve guidance conduits from aligned nanofibers: improvement of nerve regeneration through longitudinal nanogrooves on a fiber surface. , 2015, ACS applied materials & interfaces.

[45]  C. Bashur,et al.  Effect of fiber diameter and orientation on fibroblast morphology and proliferation on electrospun poly(D,L-lactic-co-glycolic acid) meshes. , 2006, Biomaterials.

[46]  Mathis O. Riehle,et al.  The use of materials patterned on a nano- and micro-metric scale in cellular engineering , 2002 .

[47]  N. Danielsen,et al.  Endogenous BDNF regulates induction of intrinsic neuronal growth programs in injured sensory neurons , 2010, Experimental Neurology.

[48]  A. Curtis,et al.  Rapid fibroblast adhesion to 27nm high polymer demixed nano-topography. , 2004, Biomaterials.

[49]  James Runt,et al.  Human foetal osteoblastic cell response to polymer-demixed nanotopographic interfaces , 2005, Journal of The Royal Society Interface.

[50]  W. Chiou,et al.  Cellular behavior on TiO2 nanonodular structures in a micro-to-nanoscale hierarchy model. , 2009, Biomaterials.

[51]  Newell R Washburn,et al.  High-throughput investigation of osteoblast response to polymer crystallinity: influence of nanometer-scale roughness on proliferation. , 2004, Biomaterials.

[52]  Derek J. Hansford,et al.  Controlled neuronal cell patterning and guided neurite growth on micropatterned nanofiber platforms , 2015 .

[53]  M. Cecchini,et al.  Neuronal differentiation on anisotropic substrates and the influence of nanotopographical noise on neurite contact guidance. , 2013, Biomaterials.

[54]  M. Guler,et al.  Neural differentiation on synthetic scaffold materials. , 2013, Biomaterials science.

[55]  Kevin J Luebke,et al.  Correlation of anisotropic cell behaviors with topographic aspect ratio. , 2009, Biomaterials.

[56]  E. Drioli,et al.  Distinct α subunits of the GABAA receptor are responsible for early hippocampal silent neuron‐related activities , 2009, Hippocampus.

[57]  N. Jeon,et al.  Multiscale patterned transplantable stem cell patches for bone tissue regeneration. , 2014, Biomaterials.

[58]  P. F. Nealey,et al.  Nanoscale topography of the basement membrane underlying the corneal epithelium of the rhesus macaque , 1999, Cell and Tissue Research.

[59]  P. Alves,et al.  Integrating human stem cell expansion and neuronal differentiation in bioreactors , 2009, BMC biotechnology.

[60]  Karim Mukhida,et al.  Expansion of Human Neural Precursor Cells in Large‐Scale Bioreactors for the Treatment of Neurodegenerative Disorders , 2008, Biotechnology progress.

[61]  I. Sagi,et al.  Introduction of correlative light and airSEMTM microscopy imaging for tissue research under ambient conditions , 2014, Scientific Reports.

[62]  Tal Dvir,et al.  Nanotechnological strategies for engineering complex tissues. , 2020, Nature nanotechnology.

[63]  Renee V. Goreham,et al.  Small surface nanotopography encourages fibroblast and osteoblast cell adhesion , 2013 .

[64]  Membrane Bioreactor for Expansion and Differentiation of Embryonic Liver Cells , 2013 .

[65]  K. Suh,et al.  Designing nanotopographical density of extracellular matrix for controlled morphology and function of human mesenchymal stem cells , 2013, Scientific Reports.

[66]  Orit Shefi,et al.  Topographic cues of nano‐scale height direct neuronal growth pattern , 2012, Biotechnology and bioengineering.

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

[68]  Surface roughness quantification of CoCrMo implant alloys. , 1999, Journal of biomedical materials research.

[69]  M. Clagett-Dame,et al.  Role of all-trans retinoic acid in neurite outgrowth and axonal elongation. , 2006, Journal of neurobiology.

[70]  Wu Ma,et al.  Neural stem cell differentiation in a cell-collagen-bioreactor culture system. , 2004, Brain research. Developmental brain research.

[71]  Xiaojun Yu,et al.  Impact of Scaffold Micro and Macro Architecture on Schwann Cell Proliferation under Dynamic Conditions in a Rotating Wall Vessel Bioreactor. , 2011, Materials science & engineering. C, Materials for biological applications.

[72]  I. Choi,et al.  Control over Neurite Directionality and Neurite Elongation on Anisotropic Micropillar Arrays. , 2016, Small.

[73]  A. Crispini,et al.  Improving the bioactivity of Zn(II)-curcumin based complexes. , 2013, Dalton transactions.

[74]  E. Drioli,et al.  Human lymphocytes cultured in 3-D bioreactors: influence of configuration on metabolite transport and reactions. , 2012, Biomaterials.

[75]  Jianping Fu,et al.  Microfabricated nanotopological surfaces for study of adhesion-dependent cell mechanosensitivity. , 2013, Small.

[76]  C. Chou,et al.  Nanofiber size-dependent sensitivity of fibroblast directionality to the methodology for scaffold alignment. , 2012, Acta biomaterialia.

[77]  C. McCaig,et al.  Guidance of CNS growth cones by substratum grooves and ridges: effects of inhibitors of the cytoskeleton, calcium channels and signal transduction pathways. , 1997, Journal of cell science.

[78]  J. Holopainen,et al.  Osteogenic and osteoclastogenic differentiation of co-cultured cells in polylactic acid-nanohydroxyapatite fiber scaffolds. , 2015, Journal of biotechnology.

[79]  J. Lahann,et al.  Physical aspects of cell culture substrates: topography, roughness, and elasticity. , 2012, Small.

[80]  A S G Curtis,et al.  In vitro reaction of endothelial cells to polymer demixed nanotopography. , 2002, Biomaterials.

[81]  Y. Liu,et al.  Effects of fiber orientation and diameter on the behavior of human dermal fibroblasts on electrospun PMMA scaffolds. , 2009, Journal of biomedical materials research. Part A.

[82]  Hongfeng Gao,et al.  Bioactive nanofibers: synergistic effects of nanotopography and chemical signaling on cell guidance. , 2007, Nano letters.

[83]  T. Blackstad,et al.  An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA 1) with particular emphasis on synaptology , 1962, The Journal of comparative neurology.

[84]  E. Drioli,et al.  PAN hollow fiber membranes elicit functional hippocampal neuronal network , 2011, Journal of Materials Science: Materials in Medicine.

[85]  C. Chen,et al.  Nano-porous Poly-L-lactic acid microtube array membranes , 2014 .

[86]  Microcarrier expansion of mouse embryonic stem cell‐derived neural stem cells in stirred bioreactors , 2011, Biotechnology and applied biochemistry.

[87]  E. Drioli,et al.  Flat and tubular membrane systems for the reconstruction of hippocampal neuronal network , 2012, Journal of tissue engineering and regenerative medicine.

[88]  A S G Curtis,et al.  Polymer-demixed nanotopography: control of fibroblast spreading and proliferation. , 2002, Tissue engineering.

[89]  Denis Wirtz,et al.  Focal adhesion size uniquely predicts cell migration , 2013, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[90]  Guang-Zhen Jin,et al.  Neurite outgrowth of dorsal root ganglia neurons is enhanced on aligned nanofibrous biopolymer scaffold with carbon nanotube coating , 2011, Neuroscience Letters.

[91]  Feng Zhang,et al.  The effects of electrospun TSF nanofiber diameter and alignment on neuronal differentiation of human embryonic stem cells. , 2012, Journal of biomedical materials research. Part A.

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

[93]  Masayoshi Ikeda,et al.  The relationship between nerve conduction velocity and fiber morphology during peripheral nerve regeneration , 2012, Brain and behavior.

[94]  J C Keller,et al.  Optimization of surface micromorphology for enhanced osteoblast responses in vitro. , 1993, The International journal of oral & maxillofacial implants.

[95]  Kam W Leong,et al.  Nanopattern-induced changes in morphology and motility of smooth muscle cells. , 2005, Biomaterials.

[96]  C. Schmidt,et al.  Selective axonal growth of embryonic hippocampal neurons according to topographic features of various sizes and shapes , 2010, International journal of nanomedicine.

[97]  J. Linderman,et al.  Integrin organization: linking adhesion ligand nanopatterns with altered cell responses. , 2011, Journal of theoretical biology.

[98]  M. J. Roberts,et al.  Engineering of Micro‐ and Nanostructured Surfaces with Anisotropic Geometries and Properties , 2012, Advanced materials.

[99]  Christopher J Murphy,et al.  The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. , 2006, Biomaterials.

[100]  Enrico Drioli,et al.  Human hepatocyte functions in a crossed hollow fiber membrane bioreactor. , 2009, Biomaterials.

[101]  Saida P. Khan,et al.  Influence of nanoscale surface roughness on neural cell attachment on silicon. , 2005, Nanomedicine : nanotechnology, biology, and medicine.

[102]  Kathryn E. Uhrich,et al.  Optimal Micropattern Dimensions Enhance Neurite Outgrowth Rates, Lengths, and Orientations , 2007, Annals of Biomedical Engineering.

[103]  L. Landmesser,et al.  Growth cone morphology and trajectory in the lumbosacral region of the chick embryo , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[104]  S. Morelli,et al.  Overstimulation of Glutamate Signals Leads to Hippocampal Transcriptional Plasticity in Hamsters , 2014, Cellular and Molecular Neurobiology.

[105]  K. Leong,et al.  Effects of nanoimprinted patterns in tissue-culture polystyrene on cell behavior. , 2005, Journal of vacuum science & technology. A, Vacuum, surfaces, and films : an official journal of the American Vacuum Society.

[106]  GeunHyung Kim,et al.  A mini-review: Cell response to microscale, nanoscale, and hierarchical patterning of surface structure. , 2014, Journal of biomedical materials research. Part B, Applied biomaterials.

[107]  N. Green,et al.  Electron microscopy and structural model of human fibronectin receptor. , 1988, The EMBO journal.

[108]  I. Choi,et al.  Cytoskeletal actin dynamics are involved in pitch-dependent neurite outgrowth on bead monolayers. , 2014, Angewandte Chemie.

[109]  P. Mattila,et al.  Filopodia: molecular architecture and cellular functions , 2008, Nature Reviews Molecular Cell Biology.

[110]  Diane Hoffman-Kim,et al.  Topography, cell response, and nerve regeneration. , 2010, Annual review of biomedical engineering.

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

[112]  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.

[113]  R. Composto,et al.  Topographic guidance of endothelial cells on silicone surfaces with micro- to nanogrooves: orientation of actin filaments and focal adhesions. , 2005, Journal of biomedical materials research. Part A.

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

[115]  E. Drioli,et al.  Membrane bioreactors for regenerative medicine: an example of the bioartificial liver , 2010 .

[116]  I. Choi,et al.  Titelbild: Pitch‐Dependent Acceleration of Neurite Outgrowth on Nanostructured Anodized Aluminum Oxide Substrates (Angew. Chem. 52/2010) , 2010 .

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

[118]  A. Mata,et al.  Fabrication of hierarchical micro–nanotopographies for cell attachment studies , 2013, Nanotechnology.

[119]  A S G Curtis,et al.  Investigating the limits of filopodial sensing: a brief report using SEM to image the interaction between 10 nm high nano‐topography and fibroblast filopodia , 2004, Cell biology international.

[120]  K. Leong,et al.  Significance of synthetic nanostructures in dictating cellular response. , 2005, Nanomedicine : nanotechnology, biology, and medicine.

[121]  Hongjun Song,et al.  The influence of fiber diameter of electrospun substrates on neural stem cell differentiation and proliferation. , 2009, Biomaterials.

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

[123]  L. Terada,et al.  Mechanotransduction and anoikis: Death and the homeless cell , 2008, Cell cycle.

[124]  Enrico Drioli,et al.  Evaluation of cell behaviour related to physico-chemical properties of polymeric membranes to be used in bioartificial organs. , 2002, Biomaterials.