Engineering ECM Complexity into Biomaterials for Directing Cell Fate

By definition, biomaterials and tissue engineering materials aim to replace, restore, and/or regenerate tissue where disease or injury has caused irreparable damage to native tissue. However, mimicking the complexity of the in vivo milieu has proved to be a serious challenge for current biomaterials. For example, one common strategy involves incorporating a short known biologically active motifs into the biomaterial to encourage cellular attachment, migration, and differentiation. In doing so, the intricacy of the dynamic in vivo environment is greatly diminished. This chapter highlights dynamic elements of the extracellular matrix (ECM) that provide critical signaling cues in vivo, the state of current biomaterial approaches, and potential approaches to incorporate more complex components into future biomaterials. The goal of this section is to introduce emerging concepts in matrix biology that have the potential to be exploited in biomaterials design, rather than being an exhaustive review of ECM dynamics.

[1]  D. Boettiger,et al.  Modulation of cell proliferation and differentiation through substrate-dependent changes in fibronectin conformation. , 1999, Molecular biology of the cell.

[2]  H. Kleinman,et al.  Neuronal laminins and their cellular receptors. , 1997, The international journal of biochemistry & cell biology.

[3]  G. I. Hatton,et al.  Fractones and other basal laminae in the hypothalamus , 2003, The Journal of comparative neurology.

[4]  I. Campbell,et al.  Structural Requirements for Biological Activity of the Ninth and Tenth FIII Domains of Human Fibronectin* , 1997, The Journal of Biological Chemistry.

[5]  V. Quaranta,et al.  Tales from the crypt[ic] sites of the extracellular matrix. , 2003, Trends in cell biology.

[6]  G Murphy,et al.  Proteolysis and cell migration: creating a path? , 1999, Current opinion in cell biology.

[7]  Klaus Schulten,et al.  A structural model for force regulated integrin binding to fibronectin's RGD-synergy site. , 2002, Matrix biology : journal of the International Society for Matrix Biology.

[8]  J. García-Verdugo,et al.  Cellular Composition and Three-Dimensional Organization of the Subventricular Germinal Zone in the Adult Mammalian Brain , 1997, The Journal of Neuroscience.

[9]  Jeffrey R Capadona,et al.  Integrin specificity and enhanced cellular activities associated with surfaces presenting a recombinant fibronectin fragment compared to RGD supports. , 2006, Biomaterials.

[10]  J. Schwarzbauer,et al.  Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. , 2005, Matrix biology : journal of the International Society for Matrix Biology.

[11]  G. I. Hatton,et al.  Anatomy of the brain neurogenic zones revisited: Fractones and the fibroblast/macrophage network , 2002, The Journal of comparative neurology.

[12]  J. C. Jones,et al.  The alpha3 laminin subunit, alpha6beta4 and alpha3beta1 integrin coordinately regulate wound healing in cultured epithelial cells and in the skin. , 1999, Journal of cell science.

[13]  G. Lynch,et al.  Integrin Subunit Gene Expression Is Regionally Differentiated in Adult Brain , 1999, The Journal of Neuroscience.

[14]  A. Metters,et al.  Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: Engineering cell-invasion characteristics , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Catherine D Reyes,et al.  The effect of integrin-specific bioactive coatings on tissue healing and implant osseointegration. , 2008, Biomaterials.

[16]  L. Lillien,et al.  BMP and FGF regulate the development of EGF-responsive neural progenitor cells. , 2000, Development.

[17]  Andrés J. García,et al.  Specific β1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum , 2004, Molecular and Cellular Neuroscience.

[18]  H. Tsai.  Shear Stress and von Willebrand Factor in Health and Disease , 2003, Seminars in thrombosis and hemostasis.

[19]  E Ruoslahti,et al.  RGD and other recognition sequences for integrins. , 1996, Annual review of cell and developmental biology.

[20]  Viola Vogel,et al.  Force-Induced Unfolding of Fibronectin in the Extracellular Matrix of Living Cells , 2007, PLoS biology.

[21]  Viola Vogel,et al.  Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. ffrench-Constant,et al.  Integrins Are Markers of Human Neural Stem Cells , 2006, Stem cells.

[23]  M. Bruss,et al.  Inhibition of mitogen-activated protein kinase kinase blocks proliferation of neural progenitor cells. , 2000, Brain research. Developmental brain research.

[24]  J. Zahm,et al.  Fibronectin and its alpha 5 beta 1-integrin receptor are involved in the wound-repair process of airway epithelium. , 1996, The American journal of physiology.

[25]  R. Fässler,et al.  Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation , 2002, The Journal of cell biology.

[26]  Lia S. Campos.  β1 integrins and neural stem cells: making sense of the extracellular environment , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  C Chothia,et al.  The molecular structure of cell adhesion molecules. , 1997, Annual review of biochemistry.

[28]  S. Dedhar,et al.  SPARC Regulates Extracellular Matrix Organization through Its Modulation of Integrin-linked Kinase Activity* , 2005, Journal of Biological Chemistry.

[29]  N. Gersdorff,et al.  Basement membrane composition in the early mouse embryo day 7 , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[30]  Catherine D Reyes,et al.  Engineering integrin-specific surfaces with a triple-helical collagen-mimetic peptide. , 2003, Journal of biomedical materials research. Part A.

[31]  J. Schwarzbauer,et al.  Accessibility to the Fibronectin Synergy Site in a 3D Matrix Regulates Engagement of α 5β 1 versus α vβ 3 Integrin Receptors , 2006 .

[32]  A. Sutherland,et al.  Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation , 2004, Development.

[33]  M. Mattson,et al.  The microenvironment of the embryonic neural stem cell: Lessons from adult niches? , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[34]  J. Miner,et al.  Laminin functions in tissue morphogenesis. , 2004, Annual review of cell and developmental biology.

[35]  L. Pénicaud,et al.  Developmental changes in integrin β-subunits in rat cerebral cortex , 1997, Neuroscience Letters.

[36]  S. Gronthos,et al.  Integrin-mediated interactions between human bone marrow stromal precursor cells and the extracellular matrix. , 2001, Bone.

[37]  D. Woodley,et al.  Laminin-5 inhibits human keratinocyte migration. , 1997, Experimental cell research.

[38]  R. Fässler,et al.  Altered synthesis of laminin 1 and absence of basement membrane component deposition in (beta)1 integrin-deficient embryoid bodies. , 2000, Journal of cell science.

[39]  Su‐Li Cheng,et al.  Bone Mineralization and Osteoblast Differentiation Are Negatively Modulated by Integrin αvβ3 , 2001 .

[40]  E. Anton,et al.  Role of integrins in the development of the cerebral cortex. , 2003, Cerebral cortex.

[41]  M. Paulsson,et al.  Absence of Basement Membranes after Targeting the LAMC1 Gene Results in Embryonic Lethality Due to Failure of Endoderm Differentiation , 1999, The Journal of cell biology.

[42]  Jeffrey A Hubbell,et al.  Materials as morphogenetic guides in tissue engineering. , 2003, Current opinion in biotechnology.

[43]  R. Linden,et al.  Structure of laminin substrate modulates cellular signaling for neuritogenesis , 2002, Journal of Cell Science.

[44]  A. Sonnenberg,et al.  Current insights into the formation and breakdown of hemidesmosomes. , 2006, Trends in cell biology.

[45]  Andrés J. García,et al.  α2β1 integrin‐specific collagen‐mimetic surfaces supporting osteoblastic differentiation , 2004 .

[46]  Lia S. Campos,et al.  β1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance , 2004, Development.

[47]  W. Park,et al.  The PPFLMLLKGSTR motif in globular domain 3 of the human laminin-5 α3 chain is crucial for integrin α3β1 binding and cell adhesion , 2005 .

[48]  V. Quaranta,et al.  Inhibitory Role of α6β4-Associated Erbb-2 and Phosphoinositide 3-Kinase in Keratinocyte Haptotactic Migration Dependent on α3β1 Integrin , 2001, Journal of Cell Biology.

[49]  Kenneth M. Yamada,et al.  Fibronectin at a glance , 2002, Journal of Cell Science.

[50]  D. Melton,et al.  "Stemness": Transcriptional Profiling of Embryonic and Adult Stem Cells , 2002, Science.

[51]  Matthew C. Phipps,et al.  The effect of collagen I mimetic peptides on mesenchymal stem cell adhesion and differentiation, and on bone formation at hydroxyapatite surfaces. , 2009, Biomaterials.

[52]  B. Roysam,et al.  Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. , 2008, Cell stem cell.

[53]  M. Mattson,et al.  β1 Integrin Maintains Integrity of the Embryonic Neocortical Stem Cell Niche , 2009, PLoS biology.

[54]  B. A. Byers,et al.  Enhanced expression of the osteoblastic phenotype on substrates that modulate fibronectin conformation and integrin receptor binding. , 2002, Biomaterials.

[55]  C. ffrench-Constant,et al.  Neural precursor cell chain migration and division are regulated through different beta1 integrins. , 1998, Development.

[56]  D. Galileo,et al.  Radial glia produce and align the ligand fibronectin during neuronal migration in the developing chick brain , 2004, The Journal of comparative neurology.

[57]  Kristi S Anseth,et al.  The effect on osteoblast function of colocalized RGD and PHSRN epitopes on PEG surfaces. , 2005, Biomaterials.

[58]  Emmanuel Dias-Neto,et al.  Discovery of a functional protein complex of netrin-4, laminin γ1 chain, and integrin α6β1 in mouse neural stem cells , 2009, Proceedings of the National Academy of Sciences.

[59]  W. Carter,et al.  Deposition of laminin 5 in epidermal wounds regulates integrin signaling and adhesion. , 2000, Current opinion in cell biology.

[60]  B. Hinz,et al.  Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix , 2007, The Journal of cell biology.

[61]  T. Shimazaki,et al.  Prospective characterization of neural stem cells by flow cytometry analysis using a combination of surface markers , 2005, Journal of neuroscience research.

[62]  Y. Tong,et al.  An integrin-specific collagen-mimetic peptide approach for optimizing Hep3B liver cell adhesion, proliferation, and cellular functions. , 2007, Tissue engineering.

[63]  V. Vogel,et al.  Coexisting conformations of fibronectin in cell culture imaged using fluorescence resonance energy transfer , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[64]  M. Humphries,et al.  Effects of collagenase-cleavage of type I collagen on alpha2beta1 integrin-mediated cell adhesion. , 1998, Journal of cell science.

[65]  Semi Kim,et al.  Regulation of Angiogenesis in Vivo by Ligation of Integrin α5β1 with the Central Cell-Binding Domain of Fibronectin , 2000 .

[66]  W. Carter,et al.  Deposition of Laminin 5 by Keratinocytes Regulates Integrin Adhesion and Signaling* , 2000, The Journal of Biological Chemistry.

[67]  W. Linke,et al.  Pulling single molecules of titin by AFM—recent advances and physiological implications , 2008, Pflügers Archiv - European Journal of Physiology.

[68]  W. Wadsworth,et al.  Assembly and tissue functions of early embryonic laminins and netrins. , 2004, Current opinion in cell biology.

[69]  E. Arikawa-Hirasawa,et al.  Novel Extracellular Matrix Structures in the Neural Stem Cell Niche Capture the Neurogenic Factor Fibroblast Growth Factor 2 from the Extracellular Milieu , 2007, Stem cells.

[70]  Mikaël M. Martino,et al.  Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability. , 2009, Biomaterials.

[71]  E Gould,et al.  Hippocampal neurogenesis in adult Old World primates. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Lia S. Campos,et al.  Regulation of neural progenitor proliferation and survival by β1 integrins , 2005, Journal of Cell Science.