Enzyme responsive GAG-based natural-synthetic hybrid hydrogel for tunable growth factor delivery and stem cell differentiation

Biomaterials

Volumn 87, Issue , 2016, Pages 104-117

  Anjum, Fraz ^a   Lienemann, Philipp S ^b,d   Metzger, Stéphanie ^b   Biernaskie, Jeff ^a,c   Kallos, Michael S ^a   Ehrbar, Martin ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF CALGARY   (Canada)

^d HARVARD UNIVERSITY   (United States)

Author keywords

Chondroitin sulphate; Factor XIII; Hydrogels; Matrix metalloproteinase (MMP); Polyethylene glycol

Indexed keywords

ALIPHATIC COMPOUNDS; BIOMIMETIC MATERIALS; BIOMIMETICS; BONE; CELL CULTURE; CELL ENGINEERING; FLOWCHARTING; HYDROGELS; MEDICAL APPLICATIONS; MODULAR CONSTRUCTION; POLYETHYLENE GLYCOLS; PROTEINS; SULFUR COMPOUNDS;

BONE MORPHOGENETIC PROTEIN-2; CHONDROITIN SULPHATE; CONCENTRATION-DEPENDENT MANNERS; DEGREE OF FUNCTIONALIZATION; FACTOR XIII; HUMAN BONE MARROW MESENCHYMAL STEM CELLS; MATRIX METALLOPROTEINASES; OSTEOGENIC DIFFERENTIATION;

STEM CELLS;

ARGINYLGLYCYLASPARTIC ACID; BIOMIMETIC MATERIAL; BLOOD CLOTTING FACTOR 13; CHONDROITIN SULFATE; ENZYME; FIBRIN; GLYCOSAMINOGLYCAN; MACROGOL; MATRIX METALLOPROTEINASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; RECOMBINANT GROWTH FACTOR; SULFATE; BIOMATERIAL; BONE MORPHOGENETIC PROTEIN 2; DELAYED RELEASE FORMULATION; HYDROGEL; MACROGOL DERIVATIVE;

ARTICLE; BONE DEVELOPMENT; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE TISSUE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CHEMICAL COMPOSITION; CONTROLLED STUDY; DRUG BINDING; DRUG DELIVERY SYSTEM; DRUG RELEASE; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYBRID; HYDROGEL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; SYNTHESIS; TISSUE REGENERATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; DELAYED RELEASE FORMULATION; DRUG EFFECTS; MESENCHYMAL STROMA CELL;

BIOCOMPATIBLE MATERIALS; BONE MORPHOGENETIC PROTEIN 2; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROITIN SULFATES; DELAYED-ACTION PREPARATIONS; HUMANS; HYDROGEL; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; POLYETHYLENE GLYCOLS;

EID: 84959010338     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2016.01.050     Document Type: Article

References (71)

1. Sui Z., King W.J., Murphy W.L. Protein-based hydrogels with tunable dynamic responses. Adv. Funct. Mater. 2008, 18:1824-1831. 10.1002/adfm.200701288.
2. DeForest C.A., Anseth K.S. Advances in bioactive hydrogels to probe and direct cell fate. Annu. Rev. Chem. Biomol. Eng. 2012, 3:421-444. 10.1146/annurev-chembioeng-062011-080945.
3. Lorentz K.M., Kontos S., Frey P., Hubbell J.A. Engineered aprotinin for improved stability of fibrin biomaterials. Biomaterials 2011, 32:430-438. 10.1016/j.biomaterials.2010.08.109.
4. Martino M.M., Tortelli F., Mochizuki M., Traub S., Ben-David D., Kuhn G.A., et al. Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci. Transl. Med. 2011, 3:100-189. 10.1126/scitranslmed.3002614.
5. Ehrbar M., Djonov V.G., Schnell C., Tschanz S.A., Martiny-Baron G., Schenk U., et al. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ. Res. 2004, 94:1124-1132. 10.1161/01.RES.0000126411.29641.08.
6. Sakiyama S.E., Schense J.C., Hubbell J.A. Incorporation of heparin-binding peptides into fibrin gels enhances neurite extension: an example of designer matrices in tissue engineering. FASEB J. 1999, 13:2214-2224.
7. Nakaji-Hirabayashi T., Kato K., Iwata H. Improvement of neural stem cell survival in collagen hydrogels by incorporating laminin-derived cell adhesive polypeptides. Bioconjug. Chem. 2012, 23:212-221. 10.1021/bc200481v.
8. Zhao L., Gwon H.J., Lim Y.M., Nho Y.C., Kim S.Y. Hyaluronic acid/chondroitin sulfate-based hydrogel prepared by gamma irradiation technique. Carbohydr. Polym. 2014, 102:598-605. 10.1016/j.carbpol.2013.11.048.
9. Park Y.D., Tirelli N., Hubbell J.A. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomater. Silver Jubil. Compend 2006, 203-210. 10.1016/B978-008045154-1.50023-X.
10. Ouasti S., Donno R., Cellesi F., Sherratt M.J., Terenghi G., Tirelli N. Network connectivity, mechanical properties and cell adhesion for hyaluronic acid/PEG hydrogels. Biomaterials 2011, 32:6456-6470. 10.1016/j.biomaterials.2011.05.044.
11. Baysal K., Aroguz A.Z., Adiguzel Z., Baysal B.M. Chitosan/alginate crosslinked hydrogels: preparation, characterization and application for cell growth purposes. Int. J. Biol. Macromol. 2013, 59:342-348. 10.1016/j.ijbiomac.2013.04.073.
12. Entcheva E., Bien H., Yin L., Chung C.Y., Farrell M., Kostov Y. Functional cardiac cell constructs on cellulose-based scaffolding. Biomaterials 2004, 25:5753-5762. 10.1016/j.biomaterials.2004.01.024.
13. Nie T., Baldwin A., Yamaguchi N., Kiick K.L. Production of heparin-functionalized hydrogels for the development of responsive and controlled growth factor delivery systems. J. Control Release 2007, 122:287-296. 10.1016/j.jconrel.2007.04.019.
14. Skardal A., Zhang J., McCoard L., Xu X., Oottamasathien S., Prestwich G.D. Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting. Tissue Eng. Part A 2010, 16:2675-2685. 10.1089/ten.tea.2009.0798.
15. Zarembinski T.I., Doty N.J., Erickson I.E., Srinivas R., Wirostko B.M., Tew W.P. Thiolated hyaluronan-based hydrogels crosslinked using oxidized glutathione: an injectable matrix designed for ophthalmic applications. Acta Biomater. 2014, 10:94-103. 10.1016/j.actbio.2013.09.029.
16. Ulijn Rein V., Bibi Nurguse, Jayawarna Vineetha, Thornton Paul D., Todd Simon J., Mart Robert J., et al. Bioresponsive hydrogels. Mater Today 2007, 10:40-48. 10.1016/S1369-7021(07)70049-4.
17. Milev P., Maurel P., Chiba A., Mevissen M., Popp S., Yamaguchi Y., et al. Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem. Biophys. Res. Commun. 1998, 247:207-212. 10.1006/bbrc.1998.8759.
18. Hayes A.J., Tudor D., Nowell M.A., Caterson B., Hughes C.E. Chondroitin sulfate sulfation motifs as putative biomarkers for isolation of articular cartilage progenitor cells. J. Histochem Cytochem 2008, 56:125-138. 10.1369/jhc.7A7320.2007.
19. Volpi N. Inhibition of human leukocyte elastase activity by chondroitin sulfates. Chem. Biol. Interact. 1997, 105:157-167. 10.1016/S0009-2797(97)00045-8.
20. Miyazaki T., Miyauchi S., Tawada A., Anada T., Matsuzaka S., Suzuki O. Oversulfated chondroitin sulfate-E binds to BMP-4 and enhances osteoblast differentiation. J. Cell Physiol. 2008, 217:769-777. 10.1002/jcp.21557.
21. Yang Shuqing, Guo Qiongyu, Shores Lucas S., Aly Ahmed, Ramakrishnan Meera, Kim Ga Hye, Lu Qiaozhi, Su Lixin, Elisseeff Jennifer H. Use of a chondroitin sulfate bioadhesive to enhance integration of bioglass particles for repairing critical-size bone defects. J. Biomed. Mater. Res. Part A 2015, 103:235-242.
22. Silva J.M., Georgi N., Costa R., Sher P., Reis R.L., van Blitterswijk C.A., et al. Nanostructured 3D constructs based on chitosan and chondroitin sulphate multilayers for cartilage tissue engineering. PLoS One 2013, 8. 10.1371/journal.pone.0055451.
23. Dawlee S., Sugandhi A., Balakrishnan B., Labarre D., Jayakrishnan A. Oxidized chondroitin sulfate-cross-linked gelatin matrixes: A new class of hydrogels. Biomacromolecules 2005, 6:2040-2048. 10.1021/bm050013a.
24. Guo Y., Yuan T., Xiao Z., Tang P., Xiao Y., Fan Y., et al. Hydrogels of collagen/chondroitin sulfate/hyaluronan interpenetrating polymer network for cartilage tissue engineering. J. Mater. Sci. Mater. Med. 2012, 23:2267-2279. 10.1007/s10856-012-4684-5.
25. Strehin I., Nahas Z., Arora K., Nguyen T., Elisseeff J. A versatile pH sensitive chondroitin sulfate-PEG tissue adhesive and hydrogel. Biomaterials 2010, 31:2788-2797. 10.1016/j.biomaterials.2009.12.033.
26. Fan H., Tao H., Wu Y., Hu Y., Yan Y., Luo Z. TGF-??3 immobilized PLGA-gelatin/chondroitin sulfate/hyaluronic acid hybrid scaffold for cartilage regeneration. J. Biomed. Mater. Res. Part A 2010, 95:982-992. 10.1002/jbm.a.32899.
27. Varghese S., Hwang N.S., Canver A.C., Theprungsirikul P., Lin D.W., Elisseeff J. Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol. 2008, 27:12-21. 10.1016/j.matbio.2007.07.002.
28. Sanborn T.J., Messersmith P.B., Barron A.E. In situ crosslinking of a biomimetic peptide-PEG hydrogel via thermally triggered activation of factor XIII. Biomaterials 2002, 23:2703-2710. 10.1016/S0142-9612(02)00002-9.
29. Jeong B., Bae Y.H., Kim S.W. Thermoreversible gelation of PEG-PLGA-PEG triblock copolymer aqueous solutions. Macromolecules 1999, 32:7064-7069. 10.1021/ma9908999.
30. Guvendiren M., Burdick J.A. Engineering synthetic hydrogel microenvironments to instruct stem cells. Curr. Opin. Biotechnol. 2013, 24:841-846. 10.1016/j.copbio.2013.03.009.
31. Tibbitt M.W., Anseth K.S. Dynamic microenvironments: the fourth dimension. Sci. Transl. Med. 2012, 4:160-224. 10.1126/scitranslmed.3004804.
32. Ehrbar M., Rizzi S.C., Schoenmakers R.G., San Miguel B., Hubbell J.A., Weber F.E., et al. Biomolecular hydrogels formed and degraded via site-specific enzymatic reactions. Biomacromolecules 2007, 8:3000-3007. 10.1021/bm070228f.
33. Ehrbar M., Sala A., Lienemann P., Ranga A., Mosiewicz K., Bittermann A., et al. Elucidating the role of matrix stiffness in 3D cell migration and remodeling. Biophys. J. 2011, 100:284-293. 10.1016/j.bpj.2010.11.082.
34. Lienemann P.S., Metzger S., Kiveliö A.S., Blanc A., Papageorgiou P., Astolfo A., Pinzer B.R., Cinelli P., Weber F.E., Schibli R., Béhé M.E.M. Longitudinal in vivo evaluation of bone regeneration by combined measurement of multi-pinhole SPECT and micro-CT for tissue engineering. Sci. Rep. 2015, 5.
35. Elisseeff J., Anseth K., Sims D., McIntosh W., Randolph M., Langer R. Transdermal photopolymerization for minimally invasive implantation. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3104-3107. 10.1073/pnas.96.6.3104.
36. Metzger S.1, Lienemann P.S., Ghayor C., Weber W., Martin I., Weber FE E.M. Modular poly(ethylene glycol) matrices for the controlled 3D-localized osteogenic differentiation of mesenchymal stem cells. Adv. Heal Mater. 2015, 4:550-558.
37. Lienemann P.S.1, Devaud Y.R., Reuten R., Simona B.R., Karlsson M., Weber W., Koch M., Lutolf M.P., Milleret V.E.M. Locally controlling mesenchymal stem cell morphogenesis by 3D PDGF-BB gradients towards the establishment of an in vitro perivascular niche. Integr. Biol. 2015, 7:101-111.
38. Ehrbar M., Rizzi S.C., Hlushchuk R., Djonov V., Zisch A.H., Hubbell J.A., et al. Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering. Biomaterials 2007, 28:3856-3866. 10.1016/j.biomaterials.2007.03.027.
39. Baldwin A.D., Kiick K.L. Reversible maleimide-thiol adducts yield glutathione-sensitive poly(ethylene glycol)-heparin hydrogels. Polym. Chem. 2012, 10.1039/c2py20576a.
40. Zustiak S.P., Leach J.B. Hydrolytically degradable poly(ethylene glycol) hydrogel scaffolds with tunable degradation and mechanical properties. Biomacromolecules 2010, 11:1348-1357. 10.1021/bm100137q.
41. Bathe M., Rutledge G.C., Grodzinsky A.J., Tidor B. A coarse-grained molecular model for glycosaminoglycans: application to chondroitin, chondroitin sulfate, and hyaluronic acid. Biophys. J. 2005, 88:3870-3887. 10.1529/biophysj.104.058800.
42. Lu S., Anseth K.S. Release behavior of high molecular weight solutes from poly(ethylene glycol)-based degradable networks. Macromolecules 2000, 33:2509-2515. 10.1021/ma9915024.
43. Canal T., Peppas N.A. Correlation between mesh size and equilibrium degree of swelling of polymeric networks. J. Biomed. Mater Res. 1989, 23:1183-1193. 10.1002/jbm.820231007.
44. Peppas N.A., Hilt J.Z., Khademhosseini A., Langer R. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv. Mater. 2006, 18:1345-1360. 10.1002/adma.200501612.
45. Brandl F., Kastner F., Gschwind R.M., Blunk T., Teßmar J., Göpferich A. Hydrogel-based drug delivery systems: comparison of drug diffusivity and release kinetics. J. Control Release 2010, 142:221-228. 10.1016/j.jconrel.2009.10.030.
46. Lustig S.R., Peppas N.A. Solute diffusion in swollen membranes. IX. Scaling laws for solute diffusion in gels. J. Appl. Polym. Sci. 1988, 36:735-747. 10.1002/app.1988.070360401.
47. Lin C.-C., Metters A.T. Hydrogels in controlled release formulations: network design and mathematical modeling. Adv. Drug Deliv. Rev. 2006, 58:1379-1408. 10.1016/j.addr.2006.09.004.
48. Papadimitropoulos A., Piccinini E., Brachat S., Braccini A., Wendt D., Barbero A., et al. Expansion of human mesenchymal stromal cells from fresh bone marrow in a 3D scaffold-based system under direct perfusion. PLoS One 2014, 9:e102359. 10.1371/journal.pone.0102359.
49. Kiss A., Horvath P., Rothballer A., Kutay U., Csucs G. Nuclear motility in glioma cells reveals a cell-line dependent role of various cytoskeletal components. PLoS One 2014, 9. 10.1371/journal.pone.0093431.
50. Raeber G.P., Lutolf M.P., Hubbell J.A. Molecularly engineered PEG hydrogels: a novel model system for proteolytically mediated cell migration. Biophys. J. 2005, 89:1374-1388. 10.1529/biophysj.104.050682.
51. Dunn G.A. Characterising a kinesis response: time averaged measures of cell speed and directional persistence. Agents Actions Suppl. 1983, 12:14-33.
52. Othmer H.G., Dunbar S.R., A W. Models of dispersal in biological systems. J. Math. Biol. 1988, 26:263-298. 10.1007/BF00277392.
53. Dickinson R.B., Tranquillo R.T. Optimal estimation of cell-movement indexes from the statistical-analysis of cell tracking data. AIChE J. 1993, 39:1995-2010.
54. Biver E., Thouverey C., Magne D., Caverzasio J. Crosstalk between tyrosine kinase receptors, GSK3 and BMP2 signaling during osteoblastic differentiation of human mesenchymal stem cells. Mol. Cell Endocrinol. 2014, 382:120-130. 10.1016/j.mce.2013.09.018.
55. Pounder R.J., Stanford M.J., Brooks P., Richards S.P., Dove A.P. Metal free thiol-maleimide "Click" reaction as a mild functionalisation strategy for degradable polymers. Chem. Commun. (Camb.) 2008, 5158-5160. 10.1039/b809167f.
56. Hoyle C.E., Bowman C.N. Thiol-ene click chemistry. Angew. Chem. Int. Ed. 2010, 49:1540-1573. 10.1002/anie.200903924.
57. Suekama T.C., Hu J., Kurokawa T., Gong J.P., Gehrke S.H. Tuning mechanical properties of chondroitin sulfate-based double-network hydrogels. Macromol. Symp. 2013, 329:9-18. 10.1002/masy.201300012.
58. Lutolf M.P., Hubbell J.A. Synthesis and physicochemical characterization of end-linked poly(ethylene glycol)-co-peptide hydrogels formed by Michael-type addition. Biomacromolecules 2003, 4:713-722. 10.1021/bm025744e.
59. Volpi N. Analytical aspects of pharmaceutical grade chondroitin sulfates. J. Pharm. Sci. 2007, 96:3168-3180. 10.1002/jps.20997.
60. Lin S., Sangaj N., Razafiarison T., Zhang C., Varghese S. Influence of physical properties of biomaterials on cellular behavior. Pharm. Res. 2011, 28:1422-1430. 10.1007/s11095-011-0378-9.
61. Liu S.Q., Tian Q., Hedrick J.L., Po Hui J.H., Rachel Ee P.L., Yang Y.Y. Biomimetic hydrogels for chondrogenic differentiation of human mesenchymal stem cells to neocartilage. Biomaterials 2010, 31:7298-7307. 10.1016/j.biomaterials.2010.06.001.
62. H1 Park, Guo X., Temenoff J.S., Tabata Y., Caplan A.I., Kasper FK M.A. Effect of swelling ratio of injectable hydrogel composites on chondrogenic differentiation of encapsulated rabbit marrow mesenchymal stem cells in vitro. Biomacromolecules 2009, 10:541-546.
63. Griffon D.J., Sedighi M.R., Schaeffer D.V., Eurell J.A., Johnson A.L. Chitosan scaffolds: interconnective pore size and cartilage engineering. Acta Biomater. 2006, 2:313-320. 10.1016/j.actbio.2005.12.007.
64. Lien S.M., Ko L.Y., Huang T.J. Effect of pore size on ECM secretion and cell growth in gelatin scaffold for articular cartilage tissue engineering. Acta Biomater. 2009, 5:670-679. 10.1016/j.actbio.2008.09.020.
65. Bryant S.J., Chowdhury T.T., Lee D.A., Bader D.L., Anseth K.S. Crosslinking density influences chondrocyte metabolism in dynamically loaded photocrosslinked poly(ethylene glycol) hydrogels. Ann. Biomed. Eng. 2004, 32:407-417. 10.1023/B:ABME.0000017535.00602.ca.
66. Khanlari A., Detamore M.S., Gehrke S.H. Increasing cross-linking efficiency of methacrylated chondroitin sulfate hydrogels by copolymerization with oligo(ethylene glycol) diacrylates. Macromolecules 2013, 46:9609-9617. 10.1021/ma401838h.
67. Raeber G.P., Lutolf M.P., Hubbell J.A. Mechanisms of 3-D migration and matrix remodeling of fibroblasts within artificial ECMs. Acta Biomater. 2007, 3:615-629. 10.1016/j.actbio.2007.03.013.
68. Wang K., Luo Y. Defined surface immobilization of glycosaminoglycan molecules for probing and modulation of cell-material interactions. Biomacromolecules 2013, 14:2373-2382. 10.1021/bm4004942.
69. Thalla P.K., Fadlallah H., Liberelle B., Lequoy P., De Crescenzo G., Merhi Y., et al. Chondroitin sulfate coatings display low platelet but high endothelial cell adhesive properties favorable for vascular implants. Biomacromolecules 2014, 15:2512-2520. 10.1021/bm5003762.
70. Sirko S., Von Holst A., Weber A., Wizenmann A., Theocharidis U., Götz M., et al. Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells 2010, 28:775-787. 10.1002/stem.309.
71. Maeda N., Fukazawa N., Hata T. The binding of chondroitin sulfate to pleiotrophin/heparin-binding growth-associated molecule is regulated by chain length and oversulfated structures. J. Biol. Chem. 2006, 281:4894-4902. 10.1074/jbc.M507750200.