Local nascent protein deposition and remodelling guide mesenchymal stromal cell mechanosensing and fate in three-dimensional hydrogels (original) (raw)
Kim, S. H., Turnbull, J. & Guimond, S. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J. Endocrinol.209, 139–151 (2011). ArticleCAS Google Scholar
Guvendiren, M. & Burdick, J. A. Engineering synthetic hydrogel microenvironments to instruct stem cells. Curr. Opin. Biotechnol.24, 841–846 (2013). ArticleCAS Google Scholar
Tibbitt, M. W. & Anseth, K. S. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol. Bioeng.103, 655–663 (2009). ArticleCAS Google Scholar
Drury, J. L. & Mooney, D. J. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials24, 4337–4351 (2003). ArticleCAS Google Scholar
Wells, R. G. The role of matrix stiffness in regulating cell behavior. Hepatology47, 1394–1400 (2008). ArticleCAS Google Scholar
Khetan, S. et al. Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat. Mater.12, 458–465 (2013). ArticleCAS Google Scholar
Schultz, K. M., Kyburz, K. A. & Anseth, K. S. Measuring dynamic cell-material interactions and remodeling during 3D human mesenchymal stem cell migration in hydrogels. Proc. Natl Acad. Sci. USA112, E3757–E3764 (2015). ArticleCAS Google Scholar
Chaudhuri, O. et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat. Mater.15, 326–334 (2016). ArticleCAS Google Scholar
Wang, H. & Heilshorn, S. C. Adaptable hydrogel networks with reversible linkages for tissue engineering. Adv. Mater.27, 3717–3736 (2015). ArticleCAS Google Scholar
Rosales, A. M. & Anseth, K. S. The design of reversible hydrogels to capture extracellular matrix dynamics. Nat. Rev. Mater.1, 15012 (2016).
Unlu, G., Levic, D. S., Melville, D. B. & Knapik, E. W. Trafficking mechanisms of extracellular matrix macromolecules: insights from vertebrate development and human diseases. Int. J. Biochem. Cell Biol.47, 57–67 (2014). ArticleCAS Google Scholar
Gattazzo, F., Urciuolo, A. & Bonaldo, P. Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochim. Biophys. Acta1840, 2506–2519 (2014). ArticleCAS Google Scholar
Kadler, K. E., Hill, A. & Canty-Laird, E. G. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr. Opin. Cell Biol.20, 495–501 (2008). ArticleCAS Google Scholar
Gjorevski, N. & Nelson, C. M. Bidirectional extracellular matrix signaling during tissue morphogenesis. Cytokine Growth Factor Rev.20, 459–465 (2009). ArticleCAS Google Scholar
McLeod, C. M. & Mauck, R. L. High fidelity visualization of cell-to-cell variation and temporal dynamics in nascent extracellular matrix formation. Sci. Rep.6, 38852 (2016). ArticleCAS Google Scholar
Bian, L., Guvendiren, M., Mauck, R. L. & Burdick, J. A. Hydrogels that mimic developmentally relevant matrix and N-cadherin interactions enhance MSC chondrogenesis. Proc. Natl Acad. Sci. USA110, 10117–10122 (2013). ArticleCAS Google Scholar
Nicodemus, G. D., Skaalure, S. C. & Bryant, S. J. Gel structure has an impact on pericellular and extracellular matrix deposition, which subsequently alters metabolic activities in chondrocyte-laden PEG hydrogels. Acta Biomater.7, 492–504 (2011). ArticleCAS Google Scholar
Huebsch, N. et al. Matrix elasticity of void-forming hydrogels controls transplanted-stem-cell-mediated bone formation. Nat. Mater.14, 1269–1277 (2015). ArticleCAS Google Scholar
Cai, R., Nakamoto, T., Kawazoe, N. & Chen, G. Influence of stepwise chondrogenesis-mimicking 3D extracellular matrix on chondrogenic differentiation of mesenchymal stem cells. Biomaterials52, 199–207 (2015). ArticleCAS Google Scholar
Ferreira, S. A. et al. Bi-directional cell–pericellular matrix interactions direct stem cell fate. Nat. Commun.9, 4049 (2018). ArticleCAS Google Scholar
Kubow, K. E. et al. Mechanical forces regulate the interactions of fibronectin and collagen I in extracellular matrix. Nat. Commun.6, 8026 (2015). ArticleCAS Google Scholar
Li, B., Moshfegh, C., Lin, Z., Albuschies, J. & Vogel, V. Mesenchymal stem cells exploit extracellular matrix as mechanotransducer. Sci. Rep.3, 2425 (2013). Article Google Scholar
Scott, L. E., Mair, D. B., Narang, J. D., Feleke, K. & Lemmon, C. A. Fibronectin fibrillogenesis facilitates mechano-dependent cell spreading, force generation, and nuclear size in human embryonic fibroblasts. Integr. Biol.7, 1454–1465 (2015). ArticleCAS Google Scholar
Daley, W. P., Peters, S. B. & Larsen, M. Extracellular matrix dynamics in development and regenerative medicine. J. Cell Sci.121, 255–264 (2008). ArticleCAS Google Scholar
Jansen, K. A., Atherton, P. & Ballestrem, C. Mechanotransduction at the cell–matrix interface. Semin. Cell Dev. Biol.71, 75–83 (2017). ArticleCAS Google Scholar
Dieterich, D. C. et al. Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging. Nat. Protoc.2, 532–540 (2007). Article Google Scholar
Caliari, S. R., Vega, S. L., Kwon, M., Soulas, E. M. & Burdick, J. A. Dimensionality and spreading influence MSC YAP/TAZ signaling in hydrogel environments. Biomaterials103, 314–323 (2016). ArticleCAS Google Scholar
Doyle, A. D. & Yamada, K. M. Mechanosensing via cell–matrix adhesions in 3D microenvironments. Exp. Cell Res.343, 60–66 (2016). ArticleCAS Google Scholar
Hytonen, V. P. & Wehrle-Haller, B. Protein conformation as a regulator of cell–matrix adhesion. Phys. Chem. Chem. Phys.16, 6342–6357 (2014). Article Google Scholar
Tuckwell, D., Calderwood, D. A., Green, L. J. & Humphries, M. J. Integrin alpha 2 I-domain is a binding site for collagens. J. Cell Sci.108, 1629–1637 (1995). CAS Google Scholar
Connelly, J. T., Petrie, T. A., Garcia, A. J. & Levenston, M. E. Fibronectin- and collagen-mimetic ligands regulate bone marrow stromal cell chondrogenesis in three-dimensional hydrogels. Eur. Cells Mater.22, 168–177 (2011). ArticleCAS Google Scholar
Keselowsky, B. G., Collard, D. M. & Garcia, A. J. Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation. Proc. Natl Acad. Sci. USA102, 5953–5957 (2005). ArticleCAS Google Scholar
Massia, S. P. & Hubbell, J. A. Vascular endothelial cell adhesion and spreading promoted by the peptide REDV of the IIICS region of plasma fibronectin is mediated by integrin alpha 4 beta 1. J. Biol. Chem.267, 14019–14026 (1992). CAS Google Scholar
Dupont, S. et al. Role of YAP/TAZ in mechanotransduction. Nature474, 179–183 (2011). ArticleCAS Google Scholar
Brusatin, G., Panciera, T., Gandin, A., Citron, A. & Piccolo, S. Biomaterials and engineered microenvironments to control YAP/TAZ-dependent cell behaviour. Nat. Mater.17, 1063–1075 (2018). ArticleCAS Google Scholar
Fogerty, F. J., Akiyama, S. K., Yamada, K. M. & Mosher, D. F. Inhibition of binding of fibronectin to matrix assembly sites by anti-integrin (alpha 5 beta 1) antibodies. J. Cell Biol.111, 699–708 (1990). ArticleCAS Google Scholar
McDonald, J. A. et al. Fibronectin’s cell-adhesive domain and an amino-terminal matrix assembly domain participate in its assembly into fibroblast pericellular matrix. J. Biol. Chem.262, 2957–2967 (1987). CAS Google Scholar
Lee, H. P., Gu, L., Mooney, D. J., Levenston, M. E. & Chaudhuri, O. Mechanical confinement regulates cartilage matrix formation by chondrocytes. Nat. Mater.16, 1243–1251 (2017). ArticleCAS Google Scholar
Cameron, A. R., Frith, J. E., Gomez, G. A., Yap, A. S. & Cooper-White, J. J. The effect of time-dependent deformation of viscoelastic hydrogels on myogenic induction and Rac1 activity in mesenchymal stem cells. Biomaterials35, 1857–1868 (2014). ArticleCAS Google Scholar
Rodell, C. B., Dusaj, N. N., Highley, C. B. & Burdick, J. A. Injectable and cytocompatible tough double-network hydrogels through tandem supramolecular and covalent crosslinking. Adv. Mater.28, 8419–8424 (2016). ArticleCAS Google Scholar
Loebel, C., Rodell, C. B., Chen, M. H. & Burdick, J. A. Shear-thinning and self-healing hydrogels as injectable therapeutics and for 3D-printing. Nat. Protoc.12, 1521–1541 (2017). ArticleCAS Google Scholar
Rodell, C. B., Kaminski, A. L. & Burdick, J. A. Rational design of network properties in guest–host assembled and shear-thinning hyaluronic acid hydrogels. Biomacromolecules14, 4125–4134 (2013). ArticleCAS Google Scholar
Dooling, L. J., Buck, M. E., Zhang, W. B. & Tirrell, D. A. Programming molecular association and viscoelastic behavior in protein networks. Adv. Mater.28, 4651–4657 (2016). ArticleCAS Google Scholar
McKinnon, D. D., Domaille, D. W., Cha, J. N. & Anseth, K. S. Biophysically defined and cytocompatible covalently adaptable networks as viscoelastic 3D cell culture systems. Adv. Mater.26, 865–872 (2014). ArticleCAS Google Scholar
Feng, Y. et al. Exo1: a new chemical inhibitor of the exocytic pathway. Proc. Natl Acad. Sci. USA100, 6469–6474 (2003). ArticleCAS Google Scholar
von Kleist, L. & Haucke, V. At the crossroads of chemistry and cell biology: inhibiting membrane traffic by small molecules. Traffic13, 495–504 (2012). ArticleCAS Google Scholar
Mishev, K., Dejonghe, W. & Russinova, E. Small molecules for dissecting endomembrane trafficking: a cross-systems view. Cell Chem. Biol.20, 475–486 (2013). CAS Google Scholar
Purcell, B. P. et al. Injectable and bioresponsive hydrogels for on-demand matrix metalloproteinase inhibition. Nat. Mater.13, 653–661 (2014). ArticleCAS Google Scholar
Wolf, K. et al. Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J. Cell Biol.201, 1069–1084 (2013). ArticleCAS Google Scholar
Sridhar, B. V. et al. Development of a cellularly degradable PEG hydrogel to promote articular cartilage extracellular matrix deposition. Adv. Healthc. Mater.4, 702–713 (2015). ArticleCAS Google Scholar
Blache, U. et al. Notch-inducing hydrogels reveal a perivascular switch of mesenchymal stem cell fate. EMBO Rep.19, e45964 (2018). ArticleCAS Google Scholar
Cosgrove, B. D. et al. N-cadherin adhesive interactions modulate matrix mechanosensing and fate commitment of mesenchymal stem cells. Nat. Mater.15, 1297–1306 (2016). ArticleCAS Google Scholar
Gjorevski, N. et al. Designer matrices for intestinal stem cell and organoid culture. Nature539, 560–564 (2016). ArticleCAS Google Scholar
Cruz-Acuna, R. et al. Synthetic hydrogels for human intestinal organoid generation and colonic wound repair. Nat. Cell Biol.19, 1326–1335 (2017). ArticleCAS Google Scholar
Hezaveh, H. et al. Encoding stem-cell-secreted extracellular matrix protein capture in two and three dimensions using protein binding peptides. Biomacromolecules19, 721–730 (2018). ArticleCAS Google Scholar
Gardner, O. F., Alini, M. & Stoddart, M. J. Mesenchymal stem cells derived from human bone marrow. Methods Mol. Biol.1340, 41–52 (2015). ArticleCAS Google Scholar
Schoen, R. C., Bentley, K. L. & Klebe, R. J. Monoclonal antibody against human fibronectin which inhibits cell attachment. Hybrid1, 99–108 (1982). ArticleCAS Google Scholar
Gramlich, W. M., Kim, I. L. & Burdick, J. A. Synthesis and orthogonal photopatterning of hyaluronic acid hydrogels with thiol-norbornene chemistry. Biomaterials34, 9803–9811 (2013). ArticleCAS Google Scholar
Wade, R. J., Bassin, E. J., Rodell, C. B. & Burdick, J. A. Protease-degradable electrospun fibrous hydrogels. Nat. Commun.6, 6639 (2015). ArticleCAS Google Scholar
Almany, L. & Seliktar, D. Biosynthetic hydrogel scaffolds made from fibrinogen and polyethylene glycol for 3D cell cultures. Biomaterials26, 2467–2477 (2005). ArticleCAS Google Scholar
Bauer, A. et al. Hydrogel substrate stress-relaxation regulates the spreading and proliferation of mouse myoblasts. Acta Biomater.62, 82–90 (2017). ArticleCAS Google Scholar
Doube, M. et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone47, 1076–1079 (2010). Article Google Scholar
Loebel, C. et al. Cross-linking chemistry of tyramine-modified hyaluronan hydrogels alters mesenchymal stem cell early attachment and behavior. Biomacromolecules18, 855–864 (2017). ArticleCAS Google Scholar
Tseng, Q. et al. Spatial organization of the extracellular matrix regulates cell–cell junction positioning. Proc. Natl Acad. Sci. USA109, 1506–1511 (2012). ArticleCAS Google Scholar