Hydrogels for protein delivery in tissue engineering

Journal of Controlled Release

Volumn 161, Issue 2, 2012, Pages 680-692

  Censi, Roberta ^a   Di Martino, Piera ^a   Vermonden, Tina ^b   Hennink, Wim E ^b  

^a UNIVERSITY OF CAMERINO   (Italy)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Controlled release; Growth factors; Hydrogels; Protein delivery; Tissue engineering

Indexed keywords

BIOACTIVE MOLECULES; BIOACTIVE PROTEINS; BIODEGRADABLE SCAFFOLD; BIOLOGICAL PROCESS; CLINICAL DEVELOPMENT; CONTROLLED RELEASE; ENVIRONMENTAL CUES; GROWTH FACTOR; IMMOBILIZATION METHOD; IN-VITRO; PROTEIN DELIVERY; REGENERATIVE MEDICINE; RELEASE MECHANISM; TISSUE DEFECTS; TISSUE ENGINEERING APPLICATIONS; TISSUE REPAIR;

BIOACTIVITY; HYDROGELS; PROTEINS; TISSUE; TISSUE ENGINEERING;

SCAFFOLDS (BIOLOGY);

ALGINIC ACID; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; BONE MORPHOGENETIC PROTEIN; CHITOSAN; COLLAGEN; DEXTRAN; EPITHELIAL GROWTH FACTOR; FIBRIN; FIBROBLAST GROWTH FACTOR 2; GELATIN; HEPARIN; HYALURONIC ACID; NERVE GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR AB; PLATELET DERIVED GROWTH FACTOR BB; POLYSACCHARIDE; SCATTER FACTOR; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULOTROPIN;

CONTROLLED RELEASE FORMULATION; COVALENT BOND; DRUG DELIVERY SYSTEM; ENCAPSULATION; EXTRACELLULAR MATRIX; HUMAN; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; REVIEW; TISSUE ENGINEERING;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; HYDROGELS; PROTEINS; TISSUE ENGINEERING;

EID: 84862648049     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.03.002     Document Type: Review

References (174)

1. E. Lavik, R. Langer, Tissue engineering: current state and perspectives, Appl. Microbiol. Biotechnol. 65 (2004) 1-8.
2. A.G. Mikos, S.W. Herring, P. Ochareon, J. Elisseeff, H.H. Lu, R. Kandel, F.J. Schoen, M. Toner, D. Mooney, A. Atala, M.E.V. Dyke, D. Kaplan, G. Vunjak-Novakovic, Engineering Complex Tissues, Tissue Eng. 12 (2006) 3307-3339.
3. E. Bell, Tissue Engineering in Perspective, in: R.P. Lanza (Ed.), Principles of Tissue Engineering, edn 2, Academic Press, San Diego, 2000.
4. S. Kobsa, W.M. Saltzman, Bioengineering approaches to controlled protein delivery, Pediatr. Res. 63 (2008) 513-519.
5. S.T. Andreadis, D.J. Geer, Biomimetic approaches to protein and gene delivery for tissue regeneration, Trends Biotechnol. 24 (2006) 331-337.
6. R. Vasita, D.S. Katti, Growth factor-delivery systems for tissue engineering: a materials perspective, Expert Rev. Med. Devices 3 (2005) 29-47.
7. E.R. Edelman, M.A. Nugent, M.J. Karnovsky, Perivascular and intravenous administration of basic fibroblast growth factor: vascular and solid organ deposition, Proc. Natl. Acad. Sci. U. S. A. 15 (1993) 1513-1517.
8. S.M. Eppler, D.L. Combs, T.D. Henry, J.J. Lopez, S.G. Ellis, J.H. Yi, B.H. Annex, E.R. McCluskey, T.F. Zioncheck, A target-mediated model to describe the pharmacokinetics and hemodynamic effects of recombinant human vascular endothelial growth factor in humans, Clin. Pharmacol. Ther. 72 (2002) 20-32.
9. S.J. Lee, Cytokine delivery and tissue engineering, Yonsei Med. J. 41 (2000) 704-719.
10. V. Balasubramanian, O. Onaca, R. Enea, D.W. Hughes, C.G. Palivan, Protein delivery: from conventional drug delivery carriers to polymeric nanoreactors, Expert Opin. Drug Deliv. 7 (2010) 63-78.
11. P. Tayalia, D.J. Mooney, Controlled growth factor delivery for tissue engineering, Adv. Mater. 21 (2009) 3269-3285.
12. U. Nöth, L. Rackwitz, A.F. Steinert, R.S. Tuan, Cell delivery therapeutics for musculoskeletal regeneration, Adv. Drug Deliv. Rev. 62 (2010) 765-783.
13. D.L. Coutu, A.-M. Yousefi, J. Galipeau, Three-dimensional porous scaffolds at the crossroads of tissue engineering and cell-based gene therapy, J. Cell. Biochem. 108 (2009) 537-546.
14. K. Ladewig, Drug delivery in soft tissue engineering, Expert Opin. Drug Deliv. 8 (2011) 1175-1188.
15. R. Censi, P.J. Fieten, P. Di Martino, W.E. Hennink, T. Vermonden, In situ forming hydrogels by tandem thermal gelling and Michael addition reaction between thermosensitive triblock copolymers and thiolated hyaluronan, Macromolecules 43 (2010) 5771-5778.
16. R. Censi, T. Vermonden, H. Deschout, K. Braeckmans, P. Di Martino, S.C. De Smedt, C.F. Van Nostrum, W.E. Hennink, Photopolymerized thermosensitive poly(HPMAlactate)-PEG-based hydrogels: effect of network design on mechanical properties, degradation, and release behavior, Biomacromolecules 11 (2010) 2143-2151.
17. R. Censi, T. Vermonden, M.J. van Steenbergen, H. Deschout, K. Braeckmans, S.C. De Smedt, C.F. van Nostrum, P. di Martino, W.E. Hennink, Photopolymerized thermosensitive hydrogels for tailorable diffusion-controlled protein delivery, J. Control. Release 140 (2009) 230-236.
18. J.A. Burdick, M. Ward, E. Liang, M.J. Young, R. Langer, Stimulation of neurite outgrowth by neurotrophins delivered from degradable hydrogels, Biomaterials 27 (2006) 452-459.
19. S. Zhang, T.C. Holmes, C.M. DiPersio, R.O. Hynes, X. Su, A. Rich, Self-complementary oligopeptide matrices support mammalian cell attachment, Biomaterials 16 (1995) 1385-1393.
20. E.A. Silva, D.J. Mooney, Effects of VEGF temporal and spatial presentation on angiogenesis, Biomaterials 31 (2010) 1235-1241.
21. R.R. Chen, E.A. Silva, W.W. Yuen, A.A. Brock, C. Fischbach, A.S. Lin, R.E. Guldberg, D.J. Mooney, Integrated approach to designing growth factor delivery systems, FASEB J. 21 (2007) 3896-3903.
22. C. Hiemstra, Z. Zhong, M.J. van Steenbergen, W.E. Hennink, J. Feijen, Release of model proteins and basic fibroblast growth factor from in situ forming degradable dextran hydrogels, J. Control. Release 122 (2007) 71-78.
23. G.W. Bos, J.J.L. Jacobs, J.W. Koten, S. Van Tomme, T. Veldhuis, C.F. van Nostrum,W. Den Otter, W.E. Hennink, In situ crosslinked biodegradable hydrogels loaded with IL-2 are effective tools for local IL-2 therapy, Eur. J. Pharm. Sci. 21 (2004) 561-567.
24. S.R. Van Tomme, B.G. De Geest, K. Braeckmans, S.C. De Smedt, F. Siepmann, J. Siepmann, C.F. Van Nostrum, W.E. Hennink, Mobility of model proteins in hydrogels composed of oppositely charged dextran microspheres studied by protein release and fluorescence recovery after photobleaching, J. Control. Release 110 (2005) 67-78.
25. Y.J. Kim, S. Choi, J.J. Koh, M. Lee, K.S. Ko, S.W. Kim, Controlled release of insulin from injectable biodegradable triblock copolymer, Pharm. Res. 18 (2001) 548-550.
26. S. Choi, M. Baudys, S. Kim, Control of blood glucose by novel GLP-1 delivery using biodegradable triblock copolymer of PLGA-PEG-PLGA in type 2 diabetic rats, Pharm. Res. 21 (2004) 827-831.
27. F.D. Van Manakker, K. Braeckmans, N.E. Morabit, S.C. De Smedt, C.F. Van Nostrum, W.E. Hennink, Protein-release behavior of self-assembled PEG-β-cyclodextrin/-PEG-cholesterol hydrogels, Adv. Funct. Mater. 19 (2009) 2992-3001.
28. C. Hiemstra, Z. Zhong, S.R. Van Tomme, M.J. van Steenbergen, J.J.L. Jacobs, W.D. Otter, W.E. Hennink, J. Feijen, In vitro and in vivo protein delivery from in situ forming poly(ethylene glycol)-poly(lactide) hydrogels, J. Control. Release 119 (2007) 320-327.
29. M. Ehrbar, R. Schoenmakers, E.H. Christen, M. Fussenegger, W. Weber, Drug-sensing hydrogels for the inducible release of biopharmaceuticals, Nat. Mater. 7 (2008) 800-804.
30. M. Lutolf, G. Raeber, A. Zisch, N. Tirelli, J. Hubbell, Cell-responsive synthetic hydrogels, Adv. Mater. 15 (2003) 888-892.
31. E.A. Phelps, N. Landázuri, P.M. Thulé, W.R. Taylor, A.J. García, Bioartificial matrices for therapeutic vascularization, Proc. Natl. Acad. Sci. U. S. A. 107 (2010) 3323-3328.
32. S.E. Sakiyama-Elbert, J.A. Hubbell, Development of fibrin derivatives for controlled release of heparin-binding growth factors, J. Control. Release 65 (2000) 389-402.
33. S.E. Sakiyama-Elbert, J.A. Hubbell, Controlled release of nerve growth factor from a heparin-containing fibrin-based cell ingrowth matrix, J. Control. Release 69 (2000) 149-158.
34. C.-C. Lin, A.T. Metters, Metal-chelating affinity hydrogels for sustained protein release, J. Biomed. Mater. Res. A 83A (2007) 954-964.
35. C.-C. Lin, P.D. Boyer, A.A. Aimetti, K.S. Anseth, Regulating MCP-1 diffusion in affinity hydrogels for enhancing immuno-isolation, J. Control. Release 142 (2010) 384-391.
36. E. Verheyen, L. Delain-Bioton, S. Van Der Wal, N. El Morabit, A. Barendregt, W.E. Hennink, C.F. Van Nostrum, Conjugation of methacrylamide groups to a model protein via a reducible linker for immobilization and subsequent triggered release from hydrogels, Macromol. Biosci. 10 (2010) 1517-1526.
37. E. Verheyen, L. Delain-Bioton, S. der Wal, N. El Morabit, W.E. Hennink, C.F. van Nostrum, Protein macromonomers for covalent immobilization and subsequent triggered release from hydrogels, J. Control. Release 148 (2010) e18-e19.
38. M.P. Lutolf, F.E. Weber, H.G. Schmoekel, J.C. Schense, T. Kohler, R. Muller, J.A. Hubbell, Repair of bone defects using synthetic mimetics of collagenous extracellular matrices, Nat. Biotechnol. 21 (2003) 513-518.
39. F.M. Chen, R. Chen, X.J. Wang, H.H. Sun, Z.F. Wu, In vitro cellular responses to scaffolds containing two microencapulated growth factors, Biomaterials 30 (2009) 5215-5224.
40. Y.-I. Chung, S.-K. Kim, Y.-K. Lee, S.-J. Park, K.-O. Cho, S.H. Yuk, G. Tae, Y.H. Kim, Efficient revascularization by VEGF administration via heparin-functionalized nanoparticle-fibrin complex, J. Control. Release 143 (2010) 282-289.
41. M.D. Baumann, C.E. Kang, J.C. Stanwick, Y. Wang, H. Kim, Y. Lapitsky, M.S. Shoichet, An injectable drug delivery platform for sustained combination therapy, J. Control. Release 138 (2009) 205-213.
42. S.R. Van Tomme, G. Storm, W.E. Hennink, In situ gelling hydrogels for pharmaceutical and biomedical applications, Int. J. Pharm. 355 (2008) 1-18.
43. C.-C. Lin, A.T. Metters, Hydrogels in controlled release formulations: network design and mathematical modeling, Adv. Drug Deliv. Rev. 58 (2006) 1379-1408.
44. B. Amsden, Solute diffusion within hydrogels. Mechanisms and models, Macromolecules 31 (1998) 8382-8395.
45. R.W. Korsmeyer, N.A. Peppas, Macromolecular and modeling aspects of swelling-controlled systems, in: T.J. Roseman, S.Z. Mansdorf (Eds.), Controlled Release Delivery Systems, Marcel Dekker, 1983, pp. 77-90.
46. J.D. Boerckel, Y.M. Kolambkar, K.M. Dupont, B.A. Uhrig, E.A. Phelps, H.Y. Stevens, A.J. García, R.E. Guldberg, Effects of protein dose and delivery system on BMP-mediated bone regeneration, Biomaterials 32 (2011) 5241-5251.
47. K.V. Brown, B. Li, T. Guda, D.S. Perrien, S. Guelcher, J.C. Wenke, Improving bone formation in a rat femur segmental defect by controlling BMP-2 release, Tissue Eng. Part A 17 (2011) 1735-1746.
48. P.L. Ritger,N.A. Peppas, A simple equation for description of solute release II. Fickian and anomalous release from swellable devices, J. Control. Release 5 (1987) 37-42.
49. L. Serra, J. Doménech, N.A. Peppas, Drug transport mechanisms and release kinetics from molecularly designed poly(acrylic acid-g-ethylene glycol) hydrogels, Biomaterials 27 (2006) 5440-5451.
50. C.S. Brazel, N.A. Peppas, Modeling of drug release from swellable polymers, Eur. J. Pharm. Biopharm. 49 (2000) 47-58.
51. W.S.R. Censi, J. Malda, G. di Dato, P.E. Burgisser, W.J.A. Dhert, C.F. van Nostrum, P. di Martino, T. Vermonden, W.E. Hennink, Printable photopolymerizable thermosensitive p(HPMA-lactate)-PEG hydrogel for tissue engineering, Adv. Funct. Mater. 21 (2011) 1833-1842.
52. L. Pescosolido, W. Schuurman, J. Malda, P. Matricardi, F. Alhaique, T. Coviello, P.R. Van Weeren, W.J.A. Dhert, W.E. Hennink, T. Vermonden, Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting, Biomacromolecules 12 (2011) 1831-1838.
53. T.M. Seck, F.P.W. Melchels, J. Feijen, D.W. Grijpma, Designed biodegradable hydrogel structures prepared by stereolithography using poly(ethylene glycol)/poly(d, l-lactide)-based resins, J. Control. Release 148 (2010) 34-41.
54. A.S. Sawhney, C.P. Pathak, J.A. Hubbell, Bioerodible hydrogels based on photopolymerized poly(ethylene glycol)-co-poly(α-hydroxy acid) diacrylate macromers, Macromolecules 26 (1993) 581-587.
55. J.A. Burdick, M.N. Mason, A.D. Hinman, K. Thorne, K.S. Anseth, Delivery of osteoinductive growth factors from degradable PEG hydrogels influences osteoblast differentiation and mineralization, J. Control. Release 83 (2002) 53-63.
56. J. Elisseeff, W. McIntosh, K. Fu, T. Blunk, R. Langer, Controlled-release of IGF-I and TGF-β1 in a photopolymerizing hydrogel for cartilage tissue engineering, J. Orthop. Res. 19 (2001) 1098-1104.
57. A.T. Metters, K.S. Anseth, C.N. Bowman, A statistical kinetic model for the bulk degradation of PLA-b-PEG-b-PLA hydrogel networks: incorporating network non-idealities, J. Phys. Chem. B 105 (2001) 8069-8076.
58. K.A. Davis, J.A. Burdick, K.S. Anseth, Photoinitiated crosslinked degradable copolymer networks for tissue engineering applications, Biomaterials 24 (2003) 2485-2495.
59. B. Jeong, Y.H. Bae, S.W. Kim, Thermoreversible gelation of PEG-PLGA-PEG triblock copolymer aqueous solutions, Macromolecules 32 (1999) 7064-7069.
60. B. Jeong, Y.H. Bae, S.W. Kim, In situ gelation of PEG-PLGA-PEG triblock copolymer aqueous solutions and degradation thereof, J. Biomed.Mater. Res. 50 (2000) 171-177.
61. P.Y. Lee, Z. Li, L. Huang, Thermosensitive hydrogel as a Tgf-β1 gene delivery vehicle enhances diabetic wound healing, Pharm. Res. 20 (2003) 1995-2000.
62. G.M. Zentner, R. Rathi, C. Shih, J.C.McRea, M.H. Seo, H. Oh, B.G. Rhee, J. Mestecky, Z. Moldoveanu, M. Morgan, S.Weitman, Biodegradable block copolymers for delivery of proteins and water-insoluble drugs, J. Control. Release 72 (2001) 203-215.
63. T. Vermonden, N.E. Fedorovich, D. van Geemen, J. Alblas, C.F. van Nostrum, W.J.A. Dhert, W.E. Hennink, Photopolymerized thermosensitive hydrogels: synthesis, degradation, and cytocompatibility, Biomacromolecules 9 (2008) 919-926.
64. T. Vermonden, S.S. Jena, D. Barriet, R. Censi, J. van der Gucht, W.E. Hennink, R.A. Siegel, Macromolecular diffusion in self-assembling biodegradable thermosensitive hydrogels, Macromolecules 43 (2009) 782-789.
65. R. Censi, S. van Putten, T. Vermonden, P. di Martino, C.F. van Nostrum, M.C. Harmsen, R.A. Bank,W.E. Hennink, The tissue response to Photopolymerized PEG-p(HPMAm-lactate)-based Hydrogels, J. Biomed.Mater. Res. A 97 A (2010) 219-229.
66. P.C.H. Hsieh, M.E. Davis, J. Gannon, C. MacGillivray, R.T. Lee, Controlled delivery of PDGF-BB for myocardial protection using injectable self-assembling peptide nanofibers, J. Clin. Invest. 116 (2006) 237-248.
67. V.F.M. Segers, T. Tokunou, L.J. Higgins, C. MacGillivray, J. Gannon, R.T. Lee, Local delivery of protease-resistant stromal cell derived factor-1 for Stem cell recruitment after myocardial infarction, Circulation 116 (2007) 1683-1692.
68. M.E. Davis, P.C.H. Hsieh, T. Takahashi, Q. Song, S. Zhang, R.D. Kamm, A.J. Grodzinsky, P. Anversa, R.T. Lee, Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8155-8160.
69. B. Balakrishnan, R. Banerjee, Biopolymer-Based Hydrogels for Cartilage Tissue Engineering, Chem. Rev. 111 (2011) 4453-4474.
70. N. Hunt, L. Grover, Cell encapsulation using biopolymer gels for regenerative medicine, Biotechnol. Lett. 32 (2010) 733-742.
71. S. Huang, X. Fu, Naturally derived materials-based cell and drug delivery systems in skin regeneration, J. Control. Release 142 (2010) 149-159.
72. S. Van Vlierberghe, P. Dubruel, E. Schacht, Biopolymer-based hydrogels as scaffolds for tissue engineering applications: a review, Biomacromolecules (2011), doi:10.1021/bm200083n.
73. M. Rinaudo, Main properties and current applications of some polysaccharides as biomaterials, Polym. Int. 57 (2008) 397-430.
74. T. Coviello, P. Matricardi, C. Marianecci, F. Alhaique, Polysaccharide hydrogels for modified release formulations, J. Control. Release 119 (2007) 5-24.
75. L. Pescosolido, T. Piro, T. Vermonden, T. Coviello, F. Alhaique, W.E. Hennink, P. Matricardi, Biodegradable IPNs based on oxidized alginate and dextran-HEMA for controlled release of proteins, Carbohydr. Polym. 86 (2011) 208-213.
76. K.H. Bouhadir, K.Y. Lee, E. Alsberg, K.L. Damm, K.W. Anderson, D.J. Mooney, Degradation of partially oxidized alginate and its potential application for tissue engineering, Biotechnol. Progr. 17 (2001) 945-950.
77. S.Y. Rabbany, J. Pastore, M. Yamamoto, T. Miller, S. Rafii, R. Aras, M. Penn, Continuous delivery of stromal cell-derived factor-1 from alginate scaffolds accelerates wound healing, Cell Transplant. 19 (2010) 399-408.
78. M. Leonard, M.R. De Boisseson, P. Hubert, F. Dalençon, E. Dellacherie, Hydrophobically modified alginate hydrogels as protein carriers with specific controlled release properties, J. Control. Release 98 (2004) 395-405.
79. A.W. Chan, R.J. Neufeld, Tuneable semi-synthetic network alginate for absorptive encapsulation and controlled release of protein therapeutics, Biomaterials 31 (2010) 9040-9047.
80. I. Freeman, A. Kedem, S. Cohen, The effect of sulfation of alginate hydrogels on the specific binding and controlled release of heparin-binding proteins, Biomaterials 29 (2008) 3260-3268.
81. M. George, T.E. Abraham, pH sensitive alginate-guar gum hydrogel for the controlled delivery of protein drugs, Int. J. Pharm. 335 (2007) 123-129.
82. H.-F. Liang,M.-H. Hong, R.-M.Ho, C.-K. Chung, Y.-H. Lin, C.-H. Chen,H.-W. Sung,Novel method using a temperature-sensitive polymer (methylcellulose) to thermally gel aqueous alginate as a ph-sensitive hydrogel, Biomacromolecules 5 (2004) 1917-1925.
83. L. Pescosolido, S. Miatto, C. Di Meo, C. Cencetti, T. Coviello, F. Alhaique, P. Matricardi, Injectable and in situ gelling hydrogels for modified protein release, Eur. Biophys. J. 39 (2010) 903-909.
84. E. Ruvinov, J. Leor, S. Cohen, The effects of controlled HGF delivery from an affinity-binding alginate biomaterial on angiogenesis and blood perfusion in a hindlimb ischemia model, Biomaterials 31 (2010) 4573-4582.
85. E.A. Silva, D.J. Mooney, Spatiotemporal control of vascular endothelial growth factor delivery from injectable hydrogels enhances angiogenesis, J. Thromb. Haemost. 5 (2007) 590-598.
86. A.D. Jenkins, P. Kratochvìl, R.F.T. Stepto, U.W Suter, Glossary of basic terms in polymer science, Pure Appl. Chem. 68 (1996) 2287.
87. S.M. Jay, B.R. Shepherd, J.W. Andrejecsk, T.R. Kyriakides, J.S. Pober, W.M. Saltzman, Dual delivery of VEGF and MCP-1 to support endothelial cell transplantation for therapeutic vascularization, Biomaterials 31 (2010) 3054-3062.
88. S.M. Jay, W.M. Saltzman, Controlled delivery of VEGF via modulation of alginate microparticle ionic crosslinking, J. Control. Release 134 (2009) 26-34.
89. E.A. Silva, E.-S. Kim, H.J. Kong, D.J. Mooney, Material-based deployment enhances efficacy of endothelial progenitor cells, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 14347-14352.
90. S.R. Van Tomme, W.E. Hennink, Biodegradable dextran hydrogels for protein delivery applications, Expert Rev. Med. Devices 4 (2007) 147-164.
91. W.N.E. van Dijk-Wolthuis, J.A.M. Hoogeboom, M.J. van Steenbergen, S.K.Y. Tsang, W.E. Hennink, Degradation and release behavior of dextran-based hydrogels, Macromolecules 30 (1997) 4639-4645.
92. R.J.H. Stenekes, O. Franssen, E.M.G. van Bommel, D.J.A. Crommelin,W.E. Hennink, The preparation of dextran microspheres in an all-aqueous system: effect of the formulation parameters on particle characteristics, Pharm. Res. 15 (1998) 557-561.
93. C.J. De Groot, J.A. Cadée, J.-W. Koten,W.E. Hennink,W. Den Otter, Therapeutic efficacy of IL-2-loaded hydrogels in a mouse tumor model, Int. J. Cancer 98 (2002) 134-140.
94. K. Vlugt-Wensink, R. de Vrueh, M. Gresnigt, C. Hoogerbrugge, S. van Buul-Offers, L. de Leede, L. Sterkman, D. Crommelin, W. Hennink, R. Verrijk, Preclinical and clinical in vitro in vivo correlation of an hgh dextran microsphere formulation, Pharm. Res. 24 (2007) 2239-2248.
95. S.G. Lévesque,M.S. Shoichet, Synthesis of enzyme-degradable, peptide-cross-linked dextran hydrogels, Bioconjug. Chem. 18 (2007) 874-885.
96. G. Sun, Y.-I. Shen, S. Kusuma, K. Fox-Talbot, C.J. Steenbergen, S. Gerecht, Functional neovascularization of biodegradable dextran hydrogels with multiple angiogenic growth factors, Biomaterials 32 (2011) 95-106.
97. F.-M. Chen, Y.-M. Zhao, H.-H. Sun, T. Jin, Q.-T. Wang, W. Zhou, Z.-F. Wu, Y. Jin, Novel glycidyl methacrylated dextran (Dex-GMA)/gelatin hydrogel scaffolds containing microspheres loaded with bone morphogenetic proteins: formulation and characteristics, J. Control. Release 118 (2007) 65-77.
98. M. Morra, Engineering of biomaterials surfaces by hyaluronan, Biomacromolecules 6 (2005) 1205-1223.
99. M. Mori, M. Yamaguchi, S. Sumitomo, Y. Takai, Hyaluronan-based biomaterials in tissue engineering, Acta Histochem. Cytochem. 37 (2004) 1-5.
100. G. Kogan, L. Šoltés, R. Stern, P. Gemeiner, Hyaluronic acid: a natural biopolymerwith a broad range of biomedical and industrial applications, Biotechnol. Lett. 29 (2007) 17-25.
101. D.D. Allison, K.J. Grande-Allen, Hyaluronan: a powerful tissue engineering tool, Tissue Eng. 12 (2006) 2131-2140.
102. J. Patterson, R. Siew, S.W. Herring, A.S.P. Lin, R. Guldberg, P.S. Stayton, Hyaluronic acid hydrogels with controlled degradation properties for oriented bone regeneration, Biomaterials 31 (2010) 6772-6781.
103. I.L. Kim, R.L. Mauck, J.A. Burdick, Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid, Biomaterials 32 (2011) 8771-8782.
104. R.A. Peattie, D.B. Pike, B. Yu, S. Cai, X.Z. Shu, G.D. Prestwich, M.A. Firpo, R.J. Fisher, Effect of gelatin on heparin regulation of cytokine release from hyaluronanbased hydrogels, Drug Deliv. 15 (2008) 389-397.
105. M.R. Kim, T.G. Park, Temperature-responsive and degradable hyaluronic acid/pluronic composite hydrogels for controlled release of human growth hormone, J. Control. Release 80 (2002) 69-77.
106. C.M. Riley, P.W. Fuegy, M.A. Firpo, X. Zheng Shu, G.D. Prestwich, R.A. Peattie, Stimulation of in vivo angiogenesis using dual growth factor-loaded crosslinked glycosaminoglycan hydrogels, Biomaterials 27 (2006) 5935-5943.
107. E. Martínez-Sanz, D.A. Ossipov, J. Hilborn, S. Larsson, K.B. Jonsson, O.P. Varghese, Bone reservoir: injectable hyaluronic acid hydrogel for minimal invasive bone augmentation, J. Control. Release 152 (2011) 232-240.
108. J.B. Leach, C.E. Schmidt, Characterization of protein release from photocrosslinkable hyaluronic acid-polyethylene glycol hydrogel tissue engineering scaffolds, Biomaterials 26 (2005) 125-135.
109. F. Lee, J.E. Chung, M. Kurisawa, An injectable hyaluronic acid-tyramine hydrogel system for protein delivery, J. Control. Release 134 (2009) 186-193.
110. S.K.Hahn, S. Jelacic, R.V.Maier, P.S. Stayton, A.S.Hoffman, Anti-inflammatory drug delivery from hyaluronic acid hydrogels, J. Biomater. Sci. Polym. Ed. 15 (2004) 1111-1119.
111. S.K. Hahn, J.S. Kim, T. Shimobouji, Injectable hyaluronic acid microhydrogels for controlled release formulation of erythropoietin, J. Biomed. Mater. Res. A 80 (2007) 916-924.
112. S.K. Hahn, E.J. Oh, H. Miyamoto, T. Shimobouji, Sustained release formulation of erythropoietin using hyaluronic acid hydrogels crosslinked by Michael addition, Int. J. Pharm. 322 (2006) 44-51.
113. S. Cai, Y. Liu, Z.S. Xiao,G.D. Prestwich, Injectable glycosaminoglycan hydrogels for controlled release of human basic fibroblast growth factor, Biomaterials 26 (2005) 6054-6067.
114. R. Elia, P.W. Fuegy, A. VanDelden, M.A. Firpo, G.D. Prestwich, R.A. Peattie, Stimulation of in vivo angiogenesis by in situ crosslinked, dual growth factor-loaded, glycosaminoglycan hydrogels, Biomaterials 31 (2010) 4630-4638.
115. K. Ono, Y. Saito, H. Yura, K. Ishikawa, A. Kurita, T. Akaike, M. Ishihara, Photocrosslinkable chitosan as a biological adhesive, J. Biomed. Mater. Res. 49 (2000) 289-295.
116. K. Obara, M. Ishihara, T. Ishizuka, M. Fujita, Y. Ozeki, T. Maehara, Y. Saito, H. Yura, T. Matsui, H. Hattori, M. Kikuchi, A. Kurita, Photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2 stimulates wound healing in healingimpaired db/db mice, Biomaterials 24 (2003) 3437-3444.
117. M. Fujita, M. Ishihara, Y. Morimoto, M. Simizu, Y. Saito, H. Yura, T. Matsui, B. Takase, H. Hattori, Y. Kanatani, M. Kikuchi, T. Maehara, Efficacy of photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2 in a rabbit model of chronic myocardial infarction, J. Surg. Res. 126 (2005) 27-33.
118. Y. Yeo,W. Geng, T. Ito, D.S. Kohane, J.A. Burdick,M. Radisic, Photocrosslinkable hydrogel for myocyte cell culture and injection, J. Biomed. Mater. Res. B 81B (2007) 312-322.
119. K. Masuoka, M. Ishihara, T. Asazuma, H. Hattori, T. Matsui, B. Takase, Y. Kanatani, M. Fujita, Y. Saito, H. Yura, K. Fujikawa, K. Nemoto, The interaction of chitosan with fibroblast growth factor-2 and its protection from inactivation, Biomaterials 26 (2005) 3277-3284.
120. K. Obara, M. Ishihara, M. Fujita, Y. Kanatani, H. Hattori, T. Matsui, B. Takase, Y. Ozeki, S. Nakamura, T. Ishizuka, S. Tominaga, S. Hiroi, T. Kawai, T. Maehara, Acceleration of wound healing in healing-impaired db/db mice with a photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2, Wound Repair Regen. 13 (2005) 390-397.
121. H. Zhang, A. Qadeer, W. Chen, In situ gelable interpenetrating double network hydrogel formulated from binary components: thiolated chitosan and oxidized dextran, Biomacromolecules 12 (2011) 1428-1437.
122. N. Bhattarai, J. Gunn, M.Q. Zhang, Chitosan-based hydrogels for controlled, localized drug delivery, Adv. Drug Deliv. Rev. 62 (2010) 83-99.
123. M. Ishihara, K. Obara, S. Nakamura, M. Fujita, K. Masuoka, Y. Kanatani, B. Takase, H. Hattori, Y. Morimoto, M. Ishihara, T. Maehara, M. Kikuchi, Chitosan hydrogel as a drug delivery carrier to control angiogenesis, J. Artif. Organs 9 (2006) 8-16.
124. M. Amidi, E.Mastrobattista, W. Jiskoot, W.E. Hennink, Chitosan-based delivery systems for protein therapeutics and antigens, Adv. Drug Deliv. Rev. 62 (2010) 59-82.
125. N.W. Turner, C.W. Jeans, K.R. Brain, C.J. Allender, V. Hlady, D.W. Britt, From 3D to 2D: a review of the molecular imprinting of proteins, Biotechnol. Progr. 22 (2006) 1474-1489.
126. S.H. De Paoli Lacerda, B. Ingber, N. Rosenzweig, Structure-release rate correlation in collagen gels containing fluorescent drug analog, Biomaterials 26 (2005) 7165-7172.
127. D.G. Wallace, J. Rosenblatt, Collagen gel systems for sustained delivery and tissue engineering, Adv. Drug Deliv. Rev. 55 (2003) 1631-1649.
128. S. Young, M.Wong, Y. Tabata, A.G. Mikos, Gelatin as a delivery vehicle for the controlled release of bioactive molecules, J. Control. Release 109 (2005) 256-274.
129. Y. Tabata, A. Nagano, Y. Ikada, Biodegradation of hydrogel carrier incorporating fibroblast growth factor, Tissue Eng. 5 (1999) 127-138.
130. Z. Patel, H. Ueda, M. Yamamoto, Y. Tabata, A. Mikos, In vitro and in vivo release of vascular endothelial growth factor from gelatin microparticles and biodegradable composite scaffolds, Pharm. Res. 25 (2008) 2370-2378.
131. M. Sutter, J. Siepmann, W.E. Hennink, W. Jiskoot, Recombinant gelatin hydrogels for the sustained release of proteins, J. Control. Release 119 (2007) 301-312.
132. H. Teles, T. Vermonden, G. Eggink, W.E. Hennink, F.A. de Wolf, Hydrogels of collagen-inspired telechelic triblock copolymers for the sustained release of proteins, J. Control. Release 147 (2010) 298-303.
133. A.H. Zisch, U. Schenk, J.C. Schense, S.E. Sakiyama-Elbert, J.A. Hubbell, Covalently conjugated VEGF-fibrin matrices for endothelialization, J. Control. Release 72 (2001) 101-113.
134. M. Ehrbar, S.M. Zeisberger, G.P. Raeber, J.A. Hubbell, C. Schnell, A.H. Zisch, The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis, Biomaterials 29 (2008) 1720-1729.
135. H.S. Yang, S.H. Bhang, J.W. Hwang, D.-I. Kim, B.-S. Kim, Delivery of basic fibroblast growth factor using heparin-conjugated fibrin for therapeutic angiogenesis, Tissue Eng. Part A 16 (2010) 2113-2119.
136. C.T. Drinnan, G. Zhang, M.A. Alexander, A.S. Pulido, L.J. Suggs, Multimodal release of transforming growth factor-β1 and the BB isoform of platelet derived growth factor from PEGylated fibrin gels, J. Control. Release 147 (2010) 180-186.
137. A.J.T. Hyatt, D. Wang, J.C. Kwok, J.W. Fawcett, K.R. Martin, Controlled release of chondroitinase ABC from fibrin gel reduces the level of inhibitory glycosaminoglycan chains in lesioned spinal cord, J. Control. Release 147 (2010) 24-29.
138. J.P. Schillemans, E. Verheyen, A. Barendregt, W.E. Hennink, C.F. Van Nostrum, Anionic and cationic dextran hydrogels for post-loading and release of proteins, J. Control. Release 150 (2011) 266-271.
139. J.P. Schillemans, W.E. Hennink, C.F. van Nostrum, The effect of network charge on the immobilization and release of proteins from chemically crosslinked dextran hydrogels, Eur. J. Pharm. Biopharm. 76 (2010) 329-335.
140. J.P. Schillemans, W.E. Hennink, C.F. van Nostrum, Charged dextran hydrogels for post-loading and release of proteins, J. Control. Release 148 (2010) e82-e83.
141. D.J. Maxwell, B.C. Hicks, S. Parsons, S.E. Sakiyama-Elbert, Development of rationally designed affinity-based drug delivery systems, Acta Biomater. 1 (2005) 101-113.
142. E.R. Edelman, E. Mathiowitz, R. Langer, M. Klagsbrun, Controlled and modulated release of basic fibroblast growth factor, Biomaterials 12 (1991) 619-626.
143. N.X. Wang, H.A. Von Recum, Affinity-based drug delivery, Macromol. Biosci. 11 (2011) 321-332.
144. K. Lee, E.A. Silva, D.J. Mooney, Growth factor delivery-based tissue engineering: general approaches and a review of recent developments, J. R. Soc. Interface 8 (2011) 153-170.
145. M.D. Wood, G.H. Borschel, S.E. Sakiyama-Elbert, Controlled release of glialderived neurotrophic factor from fibrin matrices containing an affinity-based delivery system, J. Biomed. Mater. Res. A 89A (2009) 909-918.
146. N. Yamaguchi, B.-S. Chae, L. Zhang, K.L. Kiick, E.M. Furst, Rheological characterization of polysaccharide-poly(ethylene glycol) star copolymer hydrogels, Biomacromolecules 6 (2005) 1931-1940.
147. T. Nie, A. Baldwin, N. Yamaguchi, K.L. Kiick, Production of heparin-functionalized hydrogels for the development of responsive and controlled growth factor delivery systems, J. Control. Release 122 (2007) 287-296.
148. N. Yamaguchi, L. Zhang, B.-S. Chae, C.S. Palla, E.M. Furst, K.L. Kiick, Growth factor mediated assembly of cell receptor-responsive hydrogels, J. Am. Chem. Soc. 129 (2007) 3040-3041.
149. M.J.B. Wissink, R. Beernink, J.S. Pieper, A.A. Poot, G.H.M. Engbers, T. Beugeling, W.G. van Aken, J. Feijen, Binding and release of basic fibroblast growth factor from heparinized collagen matrices, Biomaterials 22 (2001) 2291-2299.
150. M.A. Princz, H. Sheardown, Heparin-modified dendrimer cross-linked collagen matrices for the delivery of basic fibroblast growth factor (FGF-2), J. Biomater. Sci. Polym. Ed. 19 (2008) 1201-1218.
151. M. Ohta, Y. Suzuki, H. Chou, N. Ishikawa, S. Suzuki, M. Tanihara, Y. Suzuki, Y. Mizushima, M. Dezawa, C. Ide, Novel heparin/alginate gel combined with basic fibroblast growth factor promotes nerve regeneration in rat sciatic nerve, J. Biomed. Mater. Res. A 71A (2004) 661-668.
152. Y. Liu, S. Cai, X.Z. Shu, J. Shelby, G.D. Prestwich, Release of basic fibroblast growth factor from a crosslinked glycosaminoglycan hydrogel promotes wound healing, Wound Repair Regen. 15 (2007) 245-251.
153. J.J. Yoon, H.J. Chung, T.G. Park, Photo-crosslinkable and biodegradable pluronic/heparin hydrogels for local and sustained delivery of angiogenic growth factor, J. Biomed. Mater. Res. A 83A (2007) 597-605.
154. L.B. Menajovsky, Heparin-induced thrombocytopenia: clinical manifestations and management strategies, Am. J. Med. 118 (2005) 21S-30S.
155. S.M. Willerth, P.J. Johnson, D.J. Maxwell, S.R. Parsons, M.E. Doukas, S.E. Sakiyama-Elbert, Rationally designed peptides for controlled release of nerve growth factor from fibrin matrices, J. Biomed. Mater. Res. A 80A (2007) 13-23.
156. Y. Zhao, J. Zhang, X. Wang, B. Chen, Z. Xiao, C. Shi, Z. Wei, X. Hou, Q. Wang, J. Dai, The osteogenic effect of bone morphogenetic protein-2 on the collagen scaffold conjugated with antibodies, J. Control. Release 141 (2010) 30-37.
157. E. Verheyen, J.P. Schillemans, M. Van Wijk, M.A. Demeniex, W.E. Hennink, C.F. Van Nostrum, Challenges for the effective molecular imprinting of proteins, Biomaterials 32 (2011) 3008-3020.
158. A.H. Zisch, M.P. Lutolf, M. Ehrbar, G.P. Raeber, S.C. Rizzi, N. Davies, H. Schmökel, D. Bezuidenhout, V. Djonov, P. Zilla, J.A. Hubbell, Cell-demanded release of VEGF from synthetic, biointeractive cell-ingrowth matrices for vascularized tissue growth, FASEB J. 17 (2003) 2260-2262.
159. P.D. Thornton, G. McConnell, R.V. Ulijn, Enzyme responsive polymer hydrogel beads, Chem. Commun. (2005) 5913-5915.
160. M. Ehrbar, S.C. Rizzi, R. Hlushchuk, V. Djonov, A.H. Zisch, J.A. Hubbell, F.E. Weber, M.P. Lutolf, Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering, Biomaterials 28 (2007) 3856-3866.
161. F.M. Chen, Y.M. Zhao, R. Zhang, T. Jin, H.H. Sun, Z.F. Wu, Y. Jin, Periodontal regeneration using novel glycidyl methacrylated dextran (Dex-GMA)/gelatin scaffolds containing microspheres loaded with bone morphogenetic proteins, J. Control. Release 121 (2007) 81-90.
162. M. Biondi, L. Indolfi, F. Ungaro, F. Quaglia, M. La Rotonda, P. Netti, Bioactivated collagen-based scaffolds embedding protein-releasing biodegradable microspheres: tuning of protein release kinetics, J. Mater. Sci. Mater. Med. 20 (2009) 2117-2128.
163. F. Ungaro, M. Biondi, I. d'Angelo, L. Indolfi, F. Quaglia, P.A. Netti, M.I. La Rotonda, Microsphere-integrated collagen scaffolds for tissue engineering: effect of microsphere formulation and scaffold properties on protein release kinetics, J. Control. Release 113 (2006) 128-136.
164. L. Bian, D.Y. Zhai, E. Tous, R. Rai, R.L. Mauck, J.A. Burdick, Enhanced MSC chondrogenesis following delivery of TGF-β3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo, Biomaterials 32 (2011) 6425-6434.
165. Todd K. Rosengart, Leonard Y. Lee, Shailen R. Patel, Paul D. Kligfield, Peter M. Okin, Neil R. Hackett, O. Wayne Isom, Ronald G. Crystal, Six-Month Assessment of a Phase I Trial of Angiogenic Gene Therapy for the Treatment of Coronary Artery Disease Using Direct Intramyocardial Administration of an Adenovirus Vector Expressing the VEGF121 cDNA, Ann. Surg. 230 (1999) 466.
166. B. Schumacher, P. Pecher, B.U. von Specht, T. Stegmann, Induction of neoangiogenesis in ischemic myocardium by human growth factors: first clinical results of a new treatment of coronary heart disease, Circulation 97 (1998) 645-650.
167. T.D. Henry, B.H. Annex, G.R. McKendall, M.A. Azrin, J.J. Lopez, F.J. Giordano, P.K. Shah, J.T. Willerson, R.L. Benza, D.S. Berman, C.M. Gibson, A. Bajamonde, A.C. Rundle, J. Fine, E.R. McCluskey, f.t.V. Investigators, The VIVA Trial, Circulation 107 (2003) 1359-1365.
168. M. Simons, J.A. Ware, Therapeutic angiogenesis in cardiovascular disease, Nat. Rev. Drug Discov. 2 (2003) 863-871.
169. H.T. Aro, S. Govender, A.D. Patel, P. Hernigou, A.P. De Gregorio, G.I. Popescu, J.D. Golden, J. Christensen, A. Valentin, Recombinant human bone morphogenetic protein-2: a randomized trial in open tibial fractures treated with reamed nail fixation, J. Bone Joint Surg. Am. 93 (2011) 801-808.
170. S. Govender, C. Csimma, H.K. Genant, A. Valentin-Opran, Y. Amit, R. Arbel, H. Aro, D. Atar, M. Bishay, M.G. Börner, P. Chiron, P. Choong, J. Cinats, B. Courtenay, R. Feibel, B. Geulette, C. Gravel, N. Haas, M. Raschke, E. Hammacher, D. Van der Velde, P. Hardy, M. Holt, C. Josten, R.L. Ketterl, B. Lindeque, G. Lob, H. Mathevon, G. McCoy, D. Marsh, R. Miller, E. Munting, S. Oevre, L. Nordsletten, A. Patel, A. Pohl, W. Rennie, P. Reynders, P.M. Rommens, J. Rondia, W.C. Rossouw, P.J. Daneel, S. Ruff, A. Rüter, S. Santavirtal, T.A. Schidhauer, C. Gekle, R. Schnettler, D. Segal, H. Seiler, R.B. Snowdowne, J. Stapert, G. Taglang, R. Verdonik, L. Vogels, A. Weckbach, A. Wentzensen, T. Wisriewsk, Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures a prospective, controlled, randomized study of four hundred and fifty patients, J. Bone Joint Surg. Am. 84 (2002) 2123-2134.
171. A.R. Vaccaro, J.P. Lawrence, T. Patel, L.D. Katz, D.G. Anderson, J.S. Fischgrund, J. Krop, M.G. Fehlings, D. Wong, The safety and efficacy of OP-1 (rhBMP-7) as a replacement for iliac crest autograft in posterolateral lumbar arthrodesis: a long-term (>4 years) pivotal study, Spine 33 (2008) 2850-2862.
172. A.R. Vaccaro, P.G. Whang, T. Patel, F.M. Phillips, D.G. Anderson, T.J. Albert, A.S. Hilibrand, R.S. Brower, M.F. Kurd, A. Appannagari, M. Patel, J.S. Fischgrund, The safety and efficacy of OP-1 (rhBMP-7) as a replacement for iliac crest autograft for posterolateral lumbar arthrodesis: minimum 4-year follow-up of a pilot study, Spine J. 8 (2008) 457-465.
173. R.J. Laham, F.W. Sellke, E.R. Edelman, J.D. Pearlman, J.A. Ware, D.L. Brown, J.P. Gold, M. Simons, Local perivascular delivery of basic fibroblast growth factor in patients undergoing coronary bypass surgery: results of a phase I randomized, double-blind, placebo-controlled trial, Circulation 100 (1999) 1865-1871.
174. M. Ruel, R.J. Laham, J.A. Parker, M.J. Post, J.A. Ware, M. Simons, F.W. Sellke, Long-term effects of surgical angiogenic therapy with fibroblast growth factor 2 protein, J. Thorac. Cardiovasc. Surg. 124 (2002) 28-34.