A photoreversible protein-patterning approach for guiding stem cell fate in three-dimensional gels

Nature Materials

Volumn 14, Issue 5, 2015, Pages 523-531

  Deforest, Cole A ^a   Tirrell, David A ^b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETICS; CELL CULTURE; CELL IMMOBILIZATION; CELL SIGNALING; CELLS; CYTOLOGY; MOBILE SECURITY; OSTEOBLASTS; PHYSIOLOGY; PROTEINS; STEM CELLS;

BIOMIMETIC SCAFFOLDS; EXTRACELLULAR MATRIX PROTEIN; FULL-LENGTH PROTEINS; HUMAN MESENCHYMAL STEM CELLS; REVERSIBLE IMMOBILIZATION; SYNTHETIC STRATEGIES; THREE DIMENSIONAL MATRICES; THREE-DIMENSIONAL GELS;

SCAFFOLDS (BIOLOGY);

BIOMIMETIC MATERIAL; HYDROGEL; IMMOBILIZED PROTEIN; VITRONECTIN;

CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; HUMAN; HYDROGEL; MESENCHYMAL STROMA CELL; METABOLISM; OSTEOBLAST; PHOTOCHEMISTRY; TISSUE SCAFFOLD;

BIOMIMETIC MATERIALS; CELL DIFFERENTIATION; HUMANS; HYDROGELS; IMMOBILIZED PROTEINS; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS; PHOTOCHEMICAL PROCESSES; TISSUE SCAFFOLDS; VITRONECTIN;

EID: 84928953980     PISSN: 14761122     EISSN: 14764660     Source Type: Journal    
DOI: 10.1038/nmat4219     Document Type: Article

References (55)

1. DeForest, C. A. & Anseth, K. S. Advances in bioactive hydrogels to probe and direct cell fate. Annu. Rev. Chem. Biomol. 3, 421-444 (2012).
2. Langer, R. & Tirrell, D. A. Designing materials for biology and medicine. Nature 428, 487-492 (2004).
3. Lutolf, M. P., Gilbert, P. M. & Blau, H. M. Designing materials to direct stem-cell fate. Nature 462, 433-441 (2009).
4. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
5. Huebsch, N. et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nature Mater. 9, 518-526 (2010).
6. Yang, C., Tibbitt, M.W., Basta, L. & Anseth, K. S. Mechanical memory and dosing influence stem cell fate. Nature Mater. 13, 645-652 (2014).
7. Chen, C. S., Mrksich, M., Huang, S.,Whitesides, G. M. & Ingber, D. E. Geometric control of cell life and death. Science 276, 1425-1428 (1997).
8. Petersen, O.W., Ronnovjessen, L., Howlett, A. R. & Bissell, M. J. Interaction with basement-membrane serves to rapidly distinguish growth and di-erentiation pattern of normal and malignant human breast epithelial cells. Proc. Natl Acad. Sci. USA 89, 9064-9068 (1992).
9. Burdick, J. A. & Murphy,W. L. Moving from static to dynamic complexity in hydrogel design. Nature Commun. 3, 1269 (2012).
10. Lutolf, M. P. & Hubbell, J. A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nature Biotechnol. 23, 47-55 (2005).
11. Rompolas, P., Mesa, K. R. & Greco, V. Spatial organization within a niche as a determinant of stem-cell fate. Nature 502, 513-518 (2013).
12. Katz, J. S. & Burdick, J. A. Light-responsive biomaterials: Development and applications. Macromol. Biosci. 10, 339-348 (2010).
13. DeLong, S. A., Moon, J. J. &West, J. L. Covalently immobilized gradients of bFGF on hydrogel sca-olds for directed cell migration. Biomaterials 26, 3227-3234 (2005).
14. Hahn, M. S., Miller, J. S. &West, J. L. Three-dimensional biochemical and biomechanical patterning of hydrogels for guiding cell behavior. Adv. Mater. 18, 2679-2684 (2006).
15. DeForest, C. A., Polizzotti, B. D. & Anseth, K. S. Sequential click reactions for synthesizing and patterning three-dimensional cell microenvironments. Nature Mater. 8, 659-664 (2009).
16. DeForest, C. A., Sims, E. A. & Anseth, K. S. Peptide-functionalized click hydrogels with independently tunable mechanics and chemical functionality for 3D cell culture. Chem. Mater. 22, 4783-4790 (2010).
17. DeForest, C. A. & Anseth, K. S. Cytocompatible click-based hydrogels with dynamically tunable properties through orthogonal photocoupling and photodegradation reactions. Nature Chem. 3, 925-931 (2011).
18. Luo, Y. & Shoichet, M. S. A photolabile hydrogel for guided three-dimensional cell growth and migration. Nature Mater. 3, 249-253 (2004).
19. Wylie, R. G. et al. Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels. Nature Mater. 10, 799-806 (2011).
20. Adzima, B. J. et al. Spatial and temporal control of the alkyne-azide cycloaddition by photoinitiated Cu(II) reduction. Nature Chem. 3, 258-261 (2011).
21. Mosiewicz, K. A. et al. In situ cell manipulation through enzymatic hydrogel photopatterning. Nature Mater. 12, 1072-1078 (2013).
22. Kloxin, A. M., Kasko, A. M., Salinas, C. N. & Anseth, K. S. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 324, 59-63 (2009).
23. Wirkner, M. et al. Triggered cell release from materials using bioadhesive photocleavable linkers. Adv. Mater. 23, 3907-3910 (2011).
24. Gri-N, D. R. et al. Synthesis of photodegradable macromers for conjugation and release of bioactive molecules. Biomacromolecules 14, 1199-1207 (2013).
25. Kloxin, A. M., Tibbitt, M.W. & Anseth, K. S. Synthesis of photodegradable hydrogels as dynamically tunable cell culture platforms. Nature Protoc. 5, 1867-1887 (2010).
26. Fairbanks, B. D., Singh, S. P., Bowman, C. N. & Anseth, K. S. Photodegradable, photoadaptable hydrogels via radical-mediated disulfide fragmentation reaction. Macromolecules 44, 2444-2450 (2011).
27. Gri-n, D. R. & Kasko, A. M. Photodegradable macromers and hydrogels for live cell encapsulation and release. J. Am. Chem. Soc. 134, 13103-13107 (2012).
28. Azagarsamy, M. A., Alge, D. L., Radhakrishnan, S. J., Tibbitt, M.W. & Anseth, K. S. Photocontrolled nanoparticles for on-demand release of proteins. Biomacromolecules 13, 2219-2224 (2012).
29. He, M., Li, J., Tan, S.,Wang, R. & Zhang, Y. Photodegradable supramolecular hydrogels with fluorescence turn-on reporter for photomodulation of cellular microenvironments. J. Am. Chem. Soc. 135, 18718-18721 (2013).
30. DeForest, C. A. & Anseth, K. S. Photoreversible patterning of biomolecules within click-based hydrogels. Angew. Chem. Int. Ed. 51, 1816-1819 (2011).
31. Lutolf, M. P. Materials science: Cell environments programmed with light. Nature 482, 477-478 (2012).
32. Alge, D. L. & Anseth, K. S. Bioactive hydrogels: Lighting the way. Nature Mater. 12, 950-952 (2013).
33. Agard, N. J., Prescher, J. A. & Bertozzi, C. R. A strain-promoted [3C2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J. Am. Chem. Soc. 126, 15046-15047 (2004).
34. Lutolf, M. P. et al. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: Engineering cell-invasion characteristics. Proc. Natl Acad. Sci. USA 100, 5413-5418 (2003).
35. Patterson, J. & Hubbell, J. A. Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2. Biomaterials 31, 7836-7845 (2010).
36. Codelli, J. A., Baskin, J. M., Agard, N. J. & Berozzi, C. R. Second-generation difluorinated cyclooctynes for copper-free click chemistry. J. Am. Chem. Soc. 130, 11486-11493 (2008).
37. Sims, E. A., DeForest, C. A. & Anseth, K. S. A mild, large-scale synthesis of 1,3-cyclooctanedione: Expanding access to difluorinated cyclooctyne for copper-free click chemistry. Tetrahedron Lett. 52, 1871-1873 (2011).
38. Ning, X. H., Guo, J.,Wolfert, M. A. & Boons, G. J. Visualizing metabolically labeled glycoconjugates of living cells by copper-free and fast huisgen cycloadditions. Angew. Chem. Int. Ed. 47, 2253-2255 (2008).
39. Debets, M. F. et al. Aza-dibenzocyclooctynes for fast and e-cient enzyme PEGylation via copper-free (3C2) cycloaddition. Chem. Commun. 46, 97-99 (2010).
40. Tibbitt, M.W., Kloxin, A. M., Sawicki, L. A. & Anseth, K. S. Mechanical properties and degradation of chain and step-polymerized photodegradable hydrogels. Macromolecules 46, 2785-2792 (2013).
41. Dendane, N. et al. E-cient surface patterning of oligonucleotides inside a glass capillary through oxime bond formation. Bioconjug. Chem. 18, 671-676 (2007).
42. Park, S. & Yousaf, M. N. An interfacial oxime reaction to immobilize ligands and cells in patterns and gradients to photoactive surfaces. Langmuir 24, 6201-6207 (2008).
43. Woll, D. et al. Intramolecular sensitization of photocleavage of the photolabile 2-(2-nitrophenyl)propoxycarbonyl (NPPOC) protecting group: Photoproducts and photokinetics of the release of nucleosides. Chem. Eur. J. 14, 6490-6497 (2008).
44. Odian, G. G. Principles of Polymerization 4th edn (Wiley-Interscience, 2004).
45. Jevevar, S., Kunstelj, M. & Porekar, V. G. PEGylation of therapeutic proteins. Biotechnol. J. 5, 113-128 (2010).
46. Dirksen, A. & Dawson, P. E. Rapid oxime and hydrazone ligations with aromatic aldehydes for biomolecular labeling. Bioconjug. Chem. 19, 2543-2548 (2008).
47. Blanden, A. R., Mukherjee, K., Dilek, O., Loew, M. & Bane, S. L. 4-aminophenylalanine as a biocompatible nucleophilic catalyst for hydrazone ligations at low temperature and neutral pH. Bioconjug. Chem. 22, 1954-1961 (2011).
48. Zustiak, S. P. & Leach, J. B. Characterization of protein release from hydrolytically degradable poly(ethylene glycol) hydrogels. Biotechnol. Bioeng. 108, 197-206 (2011).
49. Phillies, G. D. Di-usion of bovine serum albumin in a neutral polymer solution. Biopolymers 24, 379-386 (1985).
50. Kopan, R. & Ilagan, M. X. G. The canonical Notch signaling pathway: Unfolding the activation mechanism. Cell 137, 216-233 (2009).
51. Beckstead, B. L., Santosa, D. M. & Giachelli, C. M. Mimicking cell-cell interactions at the biomaterial-cell interface for control of stem cell di-erentiation. J. Biomed. Mater. Res. A 79A, 94-103 (2006).
52. Varnum-Finney, B. et al. Immobilization of Notch ligand, Delta-1, is required for induction of Notch signaling. J. Cell Sci. 113, 4313-4318 (2000).
53. Khetan, S. et al. Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nature Mater. 12, 458-465 (2013).
54. Hayman, E. G., Pierschbacher, M. D., Ohgren, Y. & Ruoslahti, E. Serum spreading factor (vitronectin) is present at the cell surface and in tissues. Proc. Natl Acad. Sci. USA 80, 4003-4007 (1983).
55. Lin, C. C., Metters, A. T. & Anseth, K. S. Functional PEG-peptide hydrogels to modulate local inflammation induced by the pro-inflammatory cytokine TNF-. Biomaterials 30, 4907-4914 (2009).