Avidity-controlled hydrogels for injectable co-delivery of induced pluripotent stem cell-derived endothelial cells and growth factors

Journal of Controlled Release

Volumn 191, Issue , 2014, Pages 71-81

  Mulyasasmita, Widya ^a   Cai, Lei ^a,b   Dewi, Ruby E ^a   Jha, Arshi ^b,c   Ullmann, Sabrina D ^d   Luong, Richard H ^b   Huang, Ngan F ^b,c   Heilshorn, Sarah C ^a,b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY   (United States)

^c VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Endothelial cell; Hydrogel; IPSC; Protein engineering; VEGF

Indexed keywords

BIOMIMETICS; CELLS; CYTOLOGY; DISEASE CONTROL; ENDOTHELIAL CELLS; HYDROGELS; MIXING; PEPTIDES; PROTEINS; SHEAR THINNING; SOL-GELS; STARS; STEM CELLS; TISSUE REGENERATION;

HUMAN-INDUCED PLURIPOTENT STEM CELLS; INDUCED PLURIPOTENT STEM CELLS; IPSC; PERIPHERAL ARTERIAL DISEASE; PROTEIN ENGINEERING; SOL-GEL PHASE TRANSITION; VASCULAR ENDOTHELIAL GROWTH FACTOR; VEGF;

CELL ENGINEERING;

DRUG CARRIER; MACROGOL; PROLINE RICH PROTEIN; PROTEIN VARIANT; RECOMBINANT PROTEIN; VASCULOTROPIN; DELAYED RELEASE FORMULATION; HYDROGEL; MACROGOL DERIVATIVE; PROTEIN BINDING; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL ENCAPSULATION; CELL PROTECTION; CELL STRUCTURE; CELL SURVIVAL; CELL TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; DRUG DELIVERY SYSTEM; DRUG FORMULATION; ENDOTHELIUM CELL; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GEL ELECTROPHORESIS; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; KINETICS; LIMIT OF QUANTITATION; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR RECOGNITION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PEPTIDE SYNTHESIS; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PHASE TRANSITION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN SECRETION; PROTON NUCLEAR MAGNETIC RESONANCE; RECOMBINANT DNA TECHNOLOGY; STEREOSPECIFICITY; TISSUE REGENERATION; TRANSPLANTATION; ANIMAL; CELL CULTURE; CELL SHAPE; CHEMISTRY; DELAYED RELEASE FORMULATION; DISEASE MODEL; DRUG EFFECTS; ENDOTHELIAL PROGENITOR CELL; HINDLIMB; INDUCED PLURIPOTENT STEM CELL; INTRAMUSCULAR DRUG ADMINISTRATION; ISCHEMIA; MEDICINAL CHEMISTRY; METABOLISM; NECROSIS; NONOBESE DIABETIC MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHARMACEUTICS; PROCEDURES; REGENERATION; SCID MOUSE; SKELETAL MUSCLE; SOLUBILITY; TISSUE SCAFFOLD; VASCULARIZATION; VISCOSITY; YOUNG MODULUS;

ANIMALS; CELL SHAPE; CELLS, CULTURED; CHEMISTRY, PHARMACEUTICAL; DELAYED-ACTION PREPARATIONS; DISEASE MODELS, ANIMAL; ELASTIC MODULUS; ENDOTHELIAL PROGENITOR CELLS; HINDLIMB; HUMANS; HYDROGELS; INDUCED PLURIPOTENT STEM CELLS; INJECTIONS, INTRAMUSCULAR; ISCHEMIA; KINETICS; MALE; MICE, INBRED NOD; MICE, SCID; MOLECULAR WEIGHT; MUSCLE, SKELETAL; NECROSIS; POLYETHYLENE GLYCOLS; PROTEIN BINDING; RECOMBINANT PROTEINS; REGENERATION; SOLUBILITY; TECHNOLOGY, PHARMACEUTICAL; TISSUE SCAFFOLDS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VISCOSITY;

EID: 84906946730     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.05.015     Document Type: Article

References (54)

1. C.T. Wong Po Foo, J.S. Lee, W. Mulyasasmita, A. Parisi Amon, S.C. Heilshorn, Twocomponent protein-engineered physical hydrogels for cell encapsulation, Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 22067-22072.
2. H.D. Lu, M.B. Charati, I.L. Kim, J.A. Burdick, Injectable shear-thinning hydrogels engineered with a self-assembling Dock-and-Lock mechanism, Biomaterials 33 (2012) 2145-2153.
3. H.D. Lu, D.E. Soranno, C.B. Rodell, I.L. Kim, J.A. Burdick, Secondary photocrosslinking of injectable shear-thinning dock-and-lock hydrogels, Adv. Healthc. Mater. 2 (2013) 1028-1036.
4. F. Ito, K. Usui, D. Kawahara, A. Suenaga, T. Maki, S. Kidoaki, H. Suzuki, M. Taiji, M. Itoh, Y. Hayashizaki, T. Matsuda, Reversible hydrogel formation driven by protein- peptide-specific interaction and chondrocyte entrapment, Biomaterials 31 (2010) 58-66.
5. T.Z. Grove, C.O. Osuji, J.D. Forster, E.R. Dufresne, L. Regan, Stimuli-responsive smart gels realized viamodular protein design, J.Am. Chem. Soc. 132 (2010) 14024-14026.
6. J.Wang, J. Zhang, X. Zhang, H. Zhou, A protein-based hydrogel for in vitro expansion of mesenchymal stem cells, PLoS One 8 (2013) e75727.
7. W. Mulyasasmita, J.S. Lee, S.C. Heilshorn, Molecular-level engineering of protein physical hydrogels for predictive sol-gel phase behavior, Biomacromolecules 12 (2011) 3406-3411.
8. S. Hong, P.R. Leroueil, I.J. Majoros, B.G. Orr, J.R. Baker Jr., M.M. Banaszak Holl, The binding avidity of a nanoparticle-basedmultivalent targeted drug delivery platform, Chem. Biol. 14 (2007) 107-115.
9. A. Barnard, D.K. Smith, Self-assembled multivalency: dynamic ligand arrays for high-affinity binding, Angew. Chem. Int. Ed. Engl. 51 (2012) 6572-6581.
10. D. Grunstein, M. Maglinao, R. Kikkeri, M. Collot, K. Barylyuk, B. Lepenies, F. Kamena, R. Zenobi, P.H. Seeberger, Hexameric supramolecular scaffold orients carbohydrates to sense bacteria, J. Am. Chem. Soc. 133 (2011) 13957-13966.
11. N.F. Huang, J. Okogbaa, A. Babakhanyan, J.P. Cooke, Bioluminescence imaging of stem cell-based therapeutics for vascular regeneration, Theranostics 2 (2012) 346-354.
12. A.J. Rufaihah, N.F. Huang, S. Jame, J.C. Lee, H.N. Nguyen, B. Byers, A. De, J. Okogbaa, M. Rollins, R. Reijo Pera, S.S. Gambhir, J.P. Cooke, Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in amouse model of peripheral arterial disease, Arterioscler. Thromb. Vasc. Biol. 31 (2011) e72-79.
13. B.A. Aguado, W.Mulyasasmita, J. Su, K.J. Lampe, S.C. Heilshorn, Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers, Tissue Eng. A 18 (2012) 806-815.
14. C. Yan, M.E. Mackay, K. Czymmek, R.P. Nagarkar, J.P. Schneider, D.J. Pochan, Injectable solid peptide hydrogel as a cell carrier: effects of shear flow on hydrogels and cell payload, Langmuir 28 (2012) 6076-6087.
15. B.D. Olsen, J.A. Kornfield, D.A. Tirrell, Yielding behavior in injectable hydrogels from telechelic proteins, Macromolecules 43 (2010) 9094-9099.
16. M.A. Laflamme, K.Y. Chen, A.V. Naumova, V. Muskheli, J.A. Fugate, S.K. Dupras, H. Reinecke, C. Xu, M. Hassanipour, S. Police, C. O'Sullivan, L. Collins, Y. Chen, E. Minami, E.A. Gill, S. Ueno, C. Yuan, J. Gold, C.E. Murry, Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts, Nat. Biotechnol. 25 (2007) 1015-1024.
17. H. Haider, M. Ashraf, Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation, J. Mol. Cell. Cardiol. 45 (2008) 554-566.
18. S.M. Ryan, G. Mantovani, X. Wang, D.M. Haddleton, D.J. Brayden, Advances in PEGylation of important biotech molecules: delivery aspects, Expert Opin. Drug Deliv. 5 (2008) 371-383.
19. H. Sugimoto, Y. Hamano, D. Charytan, D. Cosgrove, M. Kieran, A. Sudhakar, R. Kalluri, Neutralization of circulating vascular endothelial growth factor (VEGF) by anti- VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria, J. Biol. Chem. 278 (2003) 12605-12608.
20. G. von Degenfeld, A. Banfi, M.L. Springer, R.A. Wagner, J. Jacobi, C.R. Ozawa, M.J. Merchant, J.P. Cooke, H.M. Blau, Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia, FASEB J. 20 (2006) 2657-2659.
21. J. Tongers, J.G. Roncalli, D.W. Losordo, Therapeutic angiogenesis for critical limb ischemia - microvascular therapies coming of age, Circulation 118 (2008) 9-16.
22. G.P. Fadini, C. Agostini, A. Avogaro, Autologous stemcell therapy for peripheral arterial disease. Meta-analysis and systematic review of the literature, Atherosclerosis 209 (2010) 10-17.
23. T.P. Richardson, M.C. Peters, A.B. Ennett, D.J. Mooney, Polymeric system for dual growth factor delivery, Nat. Biotechnol. 19 (2001) 1029-1034.
24. S.M. Jay, B.R. Shepherd, J.P. Bertram, J.S. Pober, W.M. Saltzman, Engineering of multifunctional gels integrating highly efficient growth factor delivery with endothelial cell transplantation, FASEB J. 22 (2008) 2949-2956.
25. H.J. Kong, E.S. Kim, Y.-C. Huang, D.J. Mooney, Design of biodegradable hydrogel for the local and sustained delivery of angiogenic plasmid DNA, Pharm. Res. 25 (2008) 1230-1238.
26. H. Layman, A.A. Rahnemai-Azar, S.M. Pham, G. Tsechpenakis, F.M. Andreopoulos, Synergistic angiogenic effect of codelivering fibroblast growth factor 2 and granulocyte-colony stimulating factor from fibrin scaffolds and bone marrow transplantation in critical limb ischemia, Tissue Eng. A 17 (2011) 243-254.
27. K. Doi, T. Ikeda, A. Marui, T. Kushibiki, Y. Arai, K. Hirose, Y. Soga, A. Iwakura, K. Ueyama, K. Yamahara, H. Itoh, K. Nishimura, Y. Tabata, M. Komeda, Enhanced angiogenesis by gelatin hydrogels incorporating basic fibroblast growth factor in rabbit model of hind limb ischemia, Heart Vessel. 22 (2007) 104-108.
28. J. Lee, S.H. Bhang, H. Park, B.-S. Kim, K.Y. Lee, Active blood vessel formation in the ischemic hindlimb mouse model using a microsphere/hydrogel combination system, Pharm. Res. 27 (2010) 767-774.
29. E. Ruvinov, J. Leor, S. Cohen, The effects of controlled HGF delivery from an affinitybinding alginate biomaterial on angiogenesis and blood perfusion in a hindlimb ischemia model, Biomaterials 31 (2010) 4573-4582.
30. M.J.Webber, J. Tongers, C.J. Newcomb, K.T. Marquardt, J. Bauersachs, D.W. Losordo, S.I. Stupp, Supramolecular nanostructures that mimic VEGF as a strategy for ischemic tissue repair, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 13438-13443.
31. P. Jonsson, M.P. Jonsson, J.O. Tegenfeldt, F. Hook, A method improving the accuracy of fluorescence recovery after photobleaching analysis, Biophys. J. 95 (2008) 5334-5348.
32. A.J. Rufaihah, N.F. Huang, J. Kim, J. Herold, K.S. Volz, T.S. Park, J.C. Lee, E.T. Zambidis, R. Reijo-Pera, J.P. Cooke, Human induced pluripotent stem cell-derived endothelial cells exhibit functional heterogeneity, Am. J. Transl. Res. 5 (2013) 21-35.
33. A. Parisi-Amon, W. Mulyasasmita, C. Chung, S.C. Heilshorn, Protein-engineered injectable hydrogel to improve retention of transplanted adipose-derived stem cells, Adv. Healthc. Mater. 2 (2013) 428-432.
34. W.P. Russ, D.M. Lowery, P. Mishra, M.B. Yaffe, R. Ranganathan, Natural-like function in artificial WW domains, Nature 437 (2005) 579-583.
35. W.A. Petka, J.L. Harden, K.P. McGrath, D. Wirtz, D.A. Tirrell, Reversible hydrogels from self-assembling artificial proteins, Science 281 (1998) 389-392.
36. M.P. Lutolf, J.A. Hubbell, Synthesis and physicochemical characterization of endlinked poly(ethylene glycol)-co-peptide hydrogels formed by Michael-type addition, Biomacromolecules 4 (2003) 713-722.
37. M.P. Lutolf, G.P. Raeber, A.H. Zisch, N. Tirelli, J.A. Hubbell, Cell-responsive synthetic hydrogels, Adv. Mater. 15 (2003) 888-892.
38. P.J. Flory, Molecular size distributions in three dimensional polymers. I. Gelation, J. Am. Chem. Soc. 63 (1941) 3083-3090.
39. W.H. Stockmayer, Theory of molecular size distribution and gel formation in branched-chain polymers, J. Chem. Phys. 11 (1943) 45-55.
40. A. Todorovska, R.C. Roovers, O. Dolezal, A.A. Kortt, H.R. Hoogenboom, P.J. Hudson, Design and application of diabodies, triabodies and tetrabodies for cancer targeting, J. Immunol. Methods 248 (2001) 47-66.
41. M.H. Zaman, L.M. Trapani, A.L. Sieminski, D. Mackellar, H. Gong, R.D. Kamm, A. Wells, D.A. Lauffenburger, P. Matsudaira, Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 10889-10894.
42. F. Brandl, F. Kastner, R.M. Gschwind, T. Blunk, J. Tessmar, A. Gopferich, Hydrogelbased drug delivery systems: comparison of drug diffusivity and release kinetics, J. Control. Release 142 (2010) 221-228.
43. V. Eremina, J.A. Jefferson, J. Kowalewska, H. Hochster, M. Haas, J. Weisstuch, C. Richardson, J.B. Kopp, M.G. Kabir, P.H. Backx, H.P. Gerber, N. Ferrara, L. Barisoni, C. E. Alpers, S.E. Quaggin, VEGF inhibition and renal thrombotic microangiopathy, N. Engl. J. Med. 358 (2008) 1129-1136.
44. Y. Fu, W.J. Kao, Drug release kinetics and transport mechanisms of non-degradable and degradable polymeric delivery systems, Expert Opin. Drug Deliv. 7 (2010) 429-444.
45. E.A. Silva, D.J. Mooney, Effects of VEGF temporal and spatial presentation on angiogenesis, Biomaterials 31 (2010) 1235-1241.
46. S. Stromblad, D.A. Cheresh, Integrins, angiogenesis and vascular cell survival, Chem. Biol. 3 (1996) 881-885.
47. F. Re, A. Zanetti, M. Sironi, N. Polentarutti, L. Lanfrancone, E. Dejana, F. Colotta, Inhibition of anchorage-dependent cell spreading triggers apoptosis in cultured human endothelial cells, J. Cell Biol. 127 (1994) 537-546.
48. E. Chavakis, S. Dimmeler, Regulation of endothelial cell survival and apoptosis during angiogenesis, Arterioscler. Thromb. Vasc. Biol. 22 (2002) 887-893.
49. J.B. Michel, Anoikis in the cardiovascular system: known and unknown extracellular mediators, Arterioscler. Thromb. Vasc. Biol. 23 (2003) 2146-2154.
50. F.G. Giancotti, E. Ruoslahti, Integrin signaling, Science 285 (1999) 1028-1032.
51. S.I. Fraley, Y. Feng, R. Krishnamurthy, D.H. Kim, A. Celedon, G.D. Longmore, D.Wirtz, A distinctive role for focal adhesion proteins in three-dimensional cell motility, Nat. Cell Biol. 12 (2010) 598-604.
52. A. Le Huu, A. Paul, L. Xu, S. Prakash, D. Shum-Tim, Recent advancements in tissue engineering for stem cell-based cardiac therapies, Ther. Deliv. 4 (2013) 503-516.
53. Z. Raval, D.W. Losordo, Cell therapy of peripheral arterial disease: fromexperimental findings to clinical trials, Circ. Res. 112 (2013) 1288-1302.
54. N. Ferrara, H.P. Gerber, J. LeCouter, The biology of VEGF and its receptors, Nat. Med. 9 (2003) 669-676.