Maintenance of neural progenitor cell stemness in 3D hydrogels requires matrix remodelling (original) (raw)

References

  1. Goldman, S. Stem and progenitor cell–based therapy of the human central nervous system. Nat. Biotechnol. 23, 862–871 (2005).
    CAS Google Scholar
  2. Chen, K. G., Mallon, B. S., McKay, R. D. G. & Robey, P. G. Human pluripotent stem cell culture: considerations for maintenance, expansion, and therapeutics. Cell Stem Cell 14, 13–26 (2014).
    CAS Google Scholar
  3. Anderson, A. J., Piltti, K. M., Hooshmand, M. J., Nishi, R. A. & Cummings, B. J. Preclinical efficacy failure of human CNS-derived stem cells for use in the pathway study of cervical spinal cord injury. Stem Cell Rep. 8, 249–263 (2017).
    Google Scholar
  4. Marsh, S. E. et al. HuCNS-SC human NSCs fail to differentiate, form ectopic clusters, and provide no cognitive benefits in a transgenic model of Alzheimer’s disease. Stem Cell Rep. 8, 235–248 (2017).
    CAS Google Scholar
  5. Azarin, S. M. & Palecek, S. P. Matrix revolutions: a trinity of defined substrates for long-term expansion of human ESCs. Cell Stem Cell 7, 7–8 (2010).
    CAS Google Scholar
  6. Dzhoyashvili, N. A., Shen, S. & Rochev, Y. A. Natural and synthetic materials for self-renewal, long-term maintenance, and differentiation of induced pluripotent stem cells. Adv. Healthc. Mater. 4, 2342–2359 (2015).
    CAS Google Scholar
  7. Lutolf, M. P., Doyonnas, R., Havenstrite, K., Koleckar, K. & Blau, H. M. Perturbation of single hematopoietic stem cell fates in artificial niches. Integr. Biol. 1, 59–69 (2009).
    CAS Google Scholar
  8. Gilbert, P. M. et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078–1081 (2010).
    Article CAS Google Scholar
  9. McDevitt, T. C. Scalable culture of human pluripotent stem cells in 3D. Proc. Natl Acad. Sci. USA 110, 20852–20853 (2013).
    CAS Google Scholar
  10. Lei, Y. & Schaffer, D. V. A fully defined and scalable 3D culture system for human pluripotent stem cell expansion and differentiation. Proc. Natl Acad. Sci. USA 110, E5039–E5048 (2013).
    CAS Google Scholar
  11. Siti-Ismail, N., Bishop, A. E., Polak, J. M. & Mantalaris, A. The benefit of human embryonic stem cell encapsulation for prolonged feeder-free maintenance. Biomaterials 29, 3946–3952 (2008).
    CAS Google Scholar
  12. Gerecht, S. et al. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc. Natl Acad. Sci. USA 104, 11298–11303 (2007).
    CAS Google Scholar
  13. Morrison, S. J. & Spradling, A. C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132, 598–611 (2008).
    CAS Google Scholar
  14. Keung, A. J., Kumar, S. & Schaffer, D. V. Presentation counts: microenvironmental regulation of stem cells by biophysical and material cues. Annu. Rev. Cell Dev. Biol. 26, 533–556 (2010).
    CAS Google Scholar
  15. Discher, D. E., Mooney, D. J. & Zandstra, P. W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673–1677 (2009).
    CAS Google Scholar
  16. Little, L., Healy, K. E. & Schaffer, D. Engineering biomaterials for synthetic neural stem cell microenvironments. Chem. Rev. 108, 1787–1796 (2008).
    CAS Google Scholar
  17. Yang, C., Tibbitt, M. W., Basta, L. & Anseth, K. S. Mechanical memory and dosing influence stem cell fate. Nat. Mater. 13, 645–652 (2014).
    CAS Google Scholar
  18. Shi, P., Shen, K., Ghassemi, S., Hone, J. & Kam, L. C. Dynamic force generation by neural stem cells. Cell. Mol. Bioeng. 2, 464–474 (2009).
    CAS Google Scholar
  19. Gershlak, J. R. et al. Mesenchymal stem cells ability to generate traction stress in response to substrate stiffness is modulated by the changing extracellular matrix composition of the heart during development. Biochem. Biophys. Res. Commun. 439, 161–166 (2013).
    CAS Google Scholar
  20. Saha, K. et al. Substrate modulus directs neural stem cell behavior. Biophys. J. 95, 4426–4438 (2008).
    CAS Google Scholar
  21. Keung, A. J., de Juan-Pardo, E. M., Schaffer, D. V. & Kumar, S. Rho GTPases mediate the mechanosensitive lineage commitment of neural stem cells. Stem Cells 29, 1886–1897 (2011).
    CAS Google Scholar
  22. Teixeira, A. I. et al. The promotion of neuronal maturation on soft substrates. Biomaterials 30, 4567–4572 (2009).
    CAS Google Scholar
  23. Leipzig, N. D. & Shoichet, M. S. The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials 30, 6867–6878 (2009).
    CAS Google Scholar
  24. Banerjee, A. et al. The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials 30, 4695–4699 (2009).
    CAS Google Scholar
  25. Baker, B. M. & Chen, C. S. Deconstructing the third dimension—How 3D culture microenvironments alter cellular cues. J. Cell Sci. 125, 3015–3024 (2012).
    CAS Google Scholar
  26. Chaudhuri, O. et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat. Mater. 15, 326–334 (2016).
    CAS Google Scholar
  27. Patel, P. N., Gobin, A. S., West, J. L. & Patrick, C. W. Poly(ethylene glycol) hydrogel system supports preadipocyte viability, adhesion, and proliferation. Tissue Eng. 11, 1498–1505 (2005).
    CAS Google Scholar
  28. Bott, K. et al. The effect of matrix characteristics on fibroblast proliferation in 3D gels. Biomaterials 31, 8454–8464 (2010).
    CAS Google Scholar
  29. Khetan, S. et al. Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat. Mater. 12, 458–465 (2013).
    CAS Google Scholar
  30. Saha, K., Irwin, E. F., Kozhukh, J., Schaffer, D. V. & Healy, K. E. Biomimetic interfacial interpenetrating polymer networks control neural stem cell behavior. J. Biomed. Mater. Res. A 81A, 240–249 (2007).
    CAS Google Scholar
  31. Mithieux, S. M. & Weiss, A. S. Elastin. Adv. Protein Chem. 70, 437–461 (2005).
    CAS Google Scholar
  32. Chung, C., Lampe, K. J. & Heilshorn, S. C. Tetrakis(hydroxymethyl) phosphonium chloride as a covalent cross-linking agent for cell encapsulation within protein-based hydrogels. Biomacromolecules 13, 3912–3916 (2012).
    CAS Google Scholar
  33. McKay, R. Stem cells in the central nervous system. Science 276, 66–71 (1997).
    CAS Google Scholar
  34. Ahmed, S. The culture of neural stem cells. J. Cell. Biochem. 106, 1–6 (2009).
    CAS Google Scholar
  35. Huebsch, N. et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9, 518–526 (2010).
    CAS Google Scholar
  36. Tong, X. & Yang, F. Sliding hydrogels with mobile molecular ligands and crosslinks as 3D stem cell niche. Adv. Mater. 28, 7257–7263 (2016).
    CAS Google Scholar
  37. Vincent, L. G. & Engler, A. J. Stem cell differentiation: Post-degradation forces kick in. Nat. Mater. 12, 384–386 (2013).
    CAS Google Scholar
  38. Gefen, A. & Margulies, S. S. Are in vivo and in situ brain tissues mechanically similar? J. Biomech. 37, 1339–1352 (2004).
    Google Scholar
  39. Taylor, Z. & Miller, K. Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus. J. Biomech. 37, 1263–1269 (2004).
    Google Scholar
  40. Lim, T. C., Toh, W. S., Wang, L.-S., Kurisawa, M. & Spector, M. The effect of injectable gelatin-hydroxyphenylpropionic acid hydrogel matrices on the proliferation, migration, differentiation and oxidative stress resistance of adult neural stem cells. Biomaterials 33, 3446–3455 (2012).
    CAS Google Scholar
  41. Zhang, J. et al. Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of β-catenin signaling. Dev. Cell 18, 472–479 (2010).
    CAS Google Scholar
  42. Karpowicz, P. et al. E-cadherin regulates neural stem cell self-renewal. J. Neurosci. 29, 3885–3896 (2009).
    CAS Google Scholar
  43. Chenn, A. & Walsh, C. A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369 (2002).
    CAS Google Scholar
  44. Straley, K. S. & Heilshorn, S. C. Independent tuning of multiple biomaterial properties using protein engineering. Soft Matter 5, 114–124 (2009).
    CAS Google Scholar
  45. Wang, H., Cai, L., Paul, A., Enejder, A. & Heilshorn, S. C. Hybrid elastin-like polypeptide–polyethylene glycol (ELP-PEG) hydrogels with improved transparency and independent control of matrix mechanics and cell ligand density. Biomacromolecules 15, 3421–3428 (2014).
    CAS Google Scholar
  46. Enejder, A., Brackmann, C. & Svedberg, F. Coherent anti-Stokes Raman scattering microscopy of cellular lipid storage. IEEE J. Sel. Top. Quantum Electron. 16, 506–515 (2010).
    CAS Google Scholar
  47. Chung, C., Pruitt, B. L. & Heilshorn, S. C. Spontaneous cardiomyocyte differentiation of mouse embryoid bodies regulated by hydrogel crosslink density. Biomater. Sci. 1, 1082–1090 (2013).
    CAS Google Scholar
  48. Jönsson, P., Jonsson, M. P., Tegenfeldt, J. O. & Höök, F. A method improving the accuracy of fluorescence recovery after photobleaching analysis. Biophys. J. 95, 5334–5348 (2008).
    Google Scholar
  49. Babu, H., Cheung, G., Kettenmann, H., Palmer, T. D. & Kempermann, G. Enriched monolayer precursor cell cultures from micro-dissected adult mouse dentate gyrus yield functional granule cell-like neurons. PLoS ONE 2, e388 (2007).
    Google Scholar
  50. Madl, C. M., Katz, L. M. & Heilshorn, S. C. Bio-orthogonally crosslinked, engineered protein hydrogels with tunable mechanics and biochemistry for cell encapsulation. Adv. Funct. Mater. 26, 3612–3620 (2016).
    CAS Google Scholar
  51. Neef, A. B. & Luedtke, N. W. Dynamic metabolic labeling of DNA in vivo with arabinosyl nucleosides. Proc. Natl Acad. Sci. USA 108, 20404–20409 (2011).
    CAS Google Scholar
  52. Salic, A. & Mitchison, T. J. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl Acad. Sci. USA 105, 2415–2420 (2008).
    CAS Google Scholar
  53. DiMarco, R. L., Dewi, R. E., Bernal, G., Kuo, C. & Heilshorn, S. C. Protein-engineered scaffolds for in vitro 3D culture of primary adult intestinal organoids. Biomater. Sci. 3, 1376–1385 (2015).
    CAS Google Scholar
  54. Moullan, N. et al. Tetracyclines disturb mitochondrial function across eukaryotic models: a call for caution in biomedical research. Cell Rep. 10, 1681–1691 (2015).
    CAS Google Scholar
  55. Roghani, M. et al. Metalloprotease-disintegrin MDC9: intracellular maturation and catalytic activity. J. Biol. Chem. 274, 3531–3540 (1999).
    CAS Google Scholar
  56. Moss, M. L., Rasmussen, F. H., Nudelman, R., Dempsey, P. J. & Williams, J. Fluorescent substrates useful as high throughput screening tools for ADAM9. Comb. Chem. High Throughput Screen. 13, 358–365 (2010).
    CAS Google Scholar
  57. Lutolf, M. P., Raeber, G. P., Zisch, A. H., Tirelli, N. & Hubbell, J. A. Cell-responsive synthetic hydrogels. Adv. Mater. 15, 888–892 (2003).
    CAS Google Scholar
  58. Rowley, J. A., Madlambayan, G. & Mooney, D. J. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20, 45–53 (1999).
    CAS Google Scholar
  59. Desai, R. M., Koshy, S. T., Hilderbrand, S. A., Mooney, D. J. & Joshi, N. S. Versatile click alginate hydrogels crosslinked via tetrazine-norbornene chemistry. Biomaterials 50, 30–37 (2015).
    CAS Google Scholar
  60. Romano, N. H., Madl, C. M. & Heilshorn, S. C. Matrix RGD ligand density and L1CAM-mediated Schwann cell interactions synergistically enhance neurite outgrowth. Acta Biomater. 11, 48–57 (2015).
    CAS Google Scholar

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