Bioinspired materials for controlling stem cell fate.

Although researchers currently have limited ability to mimic the natural stem cell microenvironment, recent work at the interface of stem biology and biomaterials science has demonstrated that control over stem cell behavior with artificial microenvironments is quite advanced. Embryonic and adult stem cells are potentially useful platforms for tissue regeneration, cell-based therapeutics, and disease-in-a-dish models for drug screening. The major challenge in this field is to reliably control stem cell behavior outside the body. Common biological control schemes often ignore physicochemical parameters that materials scientists and engineers commonly manipulate, such as substrate topography and mechanical and rheological properties. However, with appropriate attention to these parameters, researchers have designed novel synthetic microenvironments to control stem cell behavior in rather unnatural ways. In this Account, we review synthetic microenvironments that aim to overcome the limitations of natural niches rather than to mimic them. A biomimetic stem cell control strategy is often limited by an incomplete understanding of the complex signaling pathways that drive stem cell behavior from early embryogenesis to late adulthood. The stem cell extracellular environment presents a miscellany of competing biological signals that keep the cell in a state of unstable equilibrium. Using synthetic polymers, researchers have designed synthetic microenvironments with an uncluttered array of cell signals, both specific and nonspecific, that are motivated by rather than modeled after biology. These have proven useful in maintaining cell potency, studying asymmetric cell division, and controlling cellular differentiation. We discuss recent research that highlights important biomaterials properties for controlling stem cell behavior, as well as advanced processes for selecting those materials, such as combinatorial and high-throughput screening. Much of this work has utilized micro- and nanoscale fabrication tools for controlling material properties and generating diversity in both two and three dimensions. Because of their ease of synthesis and similarity to biological soft matter, hydrogels have become a biomaterial of choice for generating 3D microenvironments. In presenting these efforts within the framework of synthetic biology, we anticipate that future researchers may exploit synthetic polymers to create microenvironments that control stem cell behavior in clinically relevant ways.

[1]  K. Anseth,et al.  Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. , 2008, Nature materials.

[2]  Robert Langer,et al.  Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells , 2007, Proceedings of the National Academy of Sciences.

[3]  R. Tuan,et al.  Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[4]  D. Scadden,et al.  The stem-cell niche as an entity of action , 2006, Nature.

[5]  S. Gerecht,et al.  Mapping the Interactions among Biomaterials, Adsorbed Proteins, and Human Embryonic Stem Cells , 2009, Advanced materials.

[6]  Sabine Neuss,et al.  Assessment of stem cell/biomaterial combinations for stem cell-based tissue engineering. , 2008, Biomaterials.

[7]  Susan X. Hsiong,et al.  Differentiation stage alters matrix control of stem cells. , 2008, Journal of biomedical materials research. Part A.

[8]  Robert Langer,et al.  Advances in Biomaterials, Drug Delivery, and Bionanotechnology , 2003 .

[9]  A. Mikos,et al.  Effect of swelling ratio of injectable hydrogel composites on chondrogenic differentiation of encapsulated rabbit marrow mesenchymal stem cells in vitro. , 2009, Biomacromolecules.

[10]  Li Deng,et al.  Repair of infarcted myocardium using mesenchymal stem cell seeded small intestinal submucosa in rabbits. , 2009, Biomaterials.

[11]  Kristi S. Anseth,et al.  Photodegradable Hydrogels for Dynamic Tuning of Physical and Chemical Properties , 2009, Science.

[12]  Robert Langer,et al.  New opportunities: the use of nanotechnologies to manipulate and track stem cells. , 2008, Cell stem cell.

[13]  Krista L. Niece,et al.  Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers , 2004, Science.

[14]  Shu Chien,et al.  Combinatorial signaling microenvironments for studying stem cell fate. , 2008, Stem cells and development.

[15]  H. Blau,et al.  Perturbation of single hematopoietic stem cell fates in artificial niches. , 2009, Integrative biology : quantitative biosciences from nano to macro.

[16]  Chad A. Cowan,et al.  Marked differences in differentiation propensity among human embryonic stem cell lines , 2008, Nature Biotechnology.

[17]  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.

[18]  Matthias P Lutolf,et al.  Artificial Stem Cell Niches , 2009, Advanced materials.

[19]  D. Steindler,et al.  Temporally restricted substrate interactions direct fate and specification of neural precursors derived from embryonic stem cells. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Hubbell,et al.  Three-dimensional extracellular matrix-directed cardioprogenitor differentiation: systematic modulation of a synthetic cell-responsive PEG-hydrogel. , 2008, Biomaterials.

[21]  D. Kaufman,et al.  Multilineage Differentiation from Human Embryonic Stem Cell Lines , 2001, Stem cells.

[22]  Michael S. Goldberg,et al.  Combinatorial and rational approaches to polymer synthesis for medicine. , 2008, Advanced drug delivery reviews.

[23]  A. Khademhosseini,et al.  Controlling size, shape and homogeneity of embryoid bodies using poly(ethylene glycol) microwells. , 2007, Lab on a chip.

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

[25]  Ross A. Marklein,et al.  Homogeneous and organized differentiation within embryoid bodies induced by microsphere-mediated delivery of small molecules. , 2009, Biomaterials.

[26]  Wim E Hennink,et al.  The effect of photopolymerization on stem cells embedded in hydrogels. , 2009, Biomaterials.

[27]  Yann Barrandon,et al.  Stem cell niches in mammals. , 2007, Experimental cell research.

[28]  J. Carson Meredith Advances in combinatorial and high-throughput screening of biofunctional polymers for gene delivery, tissue engineering and anti-fouling coatings , 2009 .

[29]  A. Khademhosseini,et al.  DNA nanoparticles encapsulated in 3D tissue-engineered scaffolds enhance osteogenic differentiation of mesenchymal stem cells. , 2008, Journal of biomedical materials research. Part A.

[30]  M. Kellomäki,et al.  Comparison of biomaterials and extracellular matrices as a culture platform for multiple, independently derived human embryonic stem cell lines. , 2009, Tissue engineering. Part A.

[31]  R. Tuan,et al.  Transient exposure to transforming growth factor beta 3 improves the mechanical properties of mesenchymal stem cell-laden cartilage constructs in a density-dependent manner. , 2009, Tissue engineering. Part A.

[32]  Kendall N Houk,et al.  Accounts of Chemical Research. , 2008, Accounts of chemical research.

[33]  Christopher S. Chen,et al.  Emergence of Patterned Stem Cell Differentiation Within Multicellular Structures , 2008, Stem cells.

[34]  Baojin Fu,et al.  Accumulated Chromosomal Instability in Murine Bone Marrow Mesenchymal Stem Cells Leads to Malignant Transformation , 2006, Stem cells.

[35]  A. Wagers,et al.  No place like home: anatomy and function of the stem cell niche , 2008, Nature Reviews Molecular Cell Biology.

[36]  M. Pittenger,et al.  Multilineage potential of adult human mesenchymal stem cells. , 1999, Science.

[37]  Fabrizio Gelain,et al.  Designer Self-Assembling Peptide Nanofiber Scaffolds for Adult Mouse Neural Stem Cell 3-Dimensional Cultures , 2006, PloS one.

[38]  Yusuke Arima,et al.  Combinatorial protein display for the cell-based screening of biomaterials that direct neural stem cell differentiation. , 2007, Biomaterials.

[39]  Anthony Peters,et al.  High-throughput and combinatorial technologies for tissue engineering applications. , 2009, Tissue engineering. Part B, Reviews.

[40]  A. Khademhosseini,et al.  Microscale technologies for tissue engineering and biology. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Daniel G. Anderson,et al.  Nanoliter-scale synthesis of arrayed biomaterials and application to human embryonic stem cells , 2004, Nature Biotechnology.

[42]  J. Jansen,et al.  Effect of dual growth factor delivery on chondrogenic differentiation of rabbit marrow mesenchymal stem cells encapsulated in injectable hydrogel composites. , 2009, Journal of biomedical materials research. Part A.

[43]  H. Clevers,et al.  Stem cells, self-renewal, and differentiation in the intestinal epithelium. , 2009, Annual review of physiology.

[44]  S. Schreiber,et al.  A small molecule that directs differentiation of human ESCs into the pancreatic lineage. , 2009, Nature chemical biology.

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

[46]  J. Mao,et al.  In vitro evaluation of macroporous hydrogels to facilitate stem cell infiltration, growth, and mineralization. , 2009, Tissue engineering. Part A.

[47]  I. Bab,et al.  Distribution of fibroblastic colony-forming cells in rabbit bone marrow and assay of their osteogenic potential by anin vivo diffusion chamber method , 2006, Calcified Tissue International.

[48]  Kristi S Anseth,et al.  Macromolecular Monomers for the Synthesis of Hydrogel Niches and Their Application in Cell Encapsulation and Tissue Engineering. , 2008, Progress in polymer science.