Hydrogels for therapeutic cardiovascular angiogenesis

Advanced Drug Delivery Reviews

Volumn 96, Issue , 2016, Pages 31-39

  Rufaihah, Abdul Jalil ^a   Seliktar, Dror ^b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Biomaterial; Cell therapy; Growth factor delivery; Ischemia; Minimally invasive; Myocardial infarction

Indexed keywords

BIOMATERIALS; CARDIOLOGY; CELLS; CYTOLOGY; HISTOLOGY; TISSUE;

CELL THERAPY; GROWTH FACTOR DELIVERY; ISCHEMIA; MINIMALLY INVASIVE; MYOCARDIAL INFARCTION;

HYDROGELS;

ALGINIC ACID; CHITOSAN; FIBRIN; FIBROBLAST GROWTH FACTOR 2; HEPARIN; HYALURONIC ACID; MACROGOL; MATRIX METALLOPROTEINASE; PLATELET DERIVED GROWTH FACTOR BB; SCATTER FACTOR; VASCULOTROPIN; BIOMATERIAL; HYDROGEL; SIGNAL PEPTIDE;

ADIPOSE DERIVED STEM CELL; ANGIOGENESIS; BIOCOMPATIBILITY; CELL ENCAPSULATION; CHEMICAL MODIFICATION; COCULTURE; CONJUGATION; CONTROLLED DRUG RELEASE; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HINDLIMB; HUMAN; HYDROGEL; LIMB ISCHEMIA; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING; ADMINISTRATION AND DOSAGE; ANIMAL; CARDIOVASCULAR DISEASES; CHEMISTRY; CYTOLOGY; DISEASE MODEL; DRUG DELIVERY SYSTEM; DRUG EFFECTS; ISCHEMIA; MYOCARDIAL INFARCTION; PROCEDURES; STEM CELL; STEM CELL TRANSPLANTATION; VASCULARIZATION;

ANIMALS; BIOCOMPATIBLE MATERIALS; CARDIOVASCULAR DISEASES; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; HINDLIMB; HUMANS; HYDROGELS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISCHEMIA; MYOCARDIAL INFARCTION; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84951858657     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2015.07.003     Document Type: Review

References (97)

1. Risau W., Flamme I. Vasculogenesis. Annu. Rev. Cell Dev. Biol. 1995, 11:73-91.
2. Asahara T., Kawamoto A. Endothelial progenitor cells for postnatal vasculogenesis. Am. J. Physiol. Cell Physiol. 2004, 287:C572-C579.
3. Carmeliet P. Angiogenesis in health and disease. Nat. Med. 2003, 9:653-660.
4. Folkman J. Fundamental concepts of the angiogenic process. Curr. Mol. Med. 2003, 3:643-651.
5. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
6. Carmeliet P., Jain R.K. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011, 473:298-307.
7. Davis G.E., Senger D.R. Extracellular matrix mediates a molecular balance between vascular morphogenesis and regression. Curr. Opin. Hematol. 2008, 15:197-203.
8. Lutolf M.P., Hubbell J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol. 2005, 23:47-55.
9. Belair D.G., Le N.N., Murphy W.L. Design of growth factor sequestering biomaterials. Chem. Commun. (Camb.) 2014, 50:15651-15668.
10. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999, 13:9-22.
11. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat. Med. 2003, 9:669-676.
12. Peters M.C., Isenberg B.C., Rowley J.A., Mooney D.J. Release from alginate enhances the biological activity of vascular endothelial growth factor. J. Biomater. Sci. Polym. Ed. 1998, 9:1267-1278.
13. Elçin Y.M., Dixit V., Gitnick G. Extensive in vivo angiogenesis following controlled release of human vascular endothelial cell growth factor: implications for tissue engineering and wound healing. Artif. Organs 2001, 25:558-565.
14. Downs E.C., Robertson N.E., Riss T.L., Plunkett M.L. Calcium alginate beads as a slow-release system for delivering angiogenic molecules in vivo and in vitro. J. Cell. Physiol. 1992, 152:422-429.
15. Lee K.Y., Peters M.C., Mooney D.J. Comparison of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in SCID mice. J. Control. Release 2003, 87:49-56.
16. Lee K.Y., Peters M.C., Anderson K.W., Mooney D.J. Controlled growth factor release from synthetic extracellular matrices. Nature 2000, 408:998-1000.
17. Lee R.J., Springer M.L., Blanco-Bose W.E., Shaw R., Ursell P.C., Blau H.M. VEGF gene delivery to myocardium: deleterious effects of unregulated expression. Circulation 2000, 102:898-901.
18. Horowitz J.R., Rivard A., van der Zee R., Hariawala M., Sheriff D.D., Esakof D.D., Chaudhry G.M., Symes J.F., Isner J.M. Vascular endothelial growth factor/vascular permeability factor produces nitric oxide-dependent hypotension. Evidence for a maintenance role in quiescent adult endothelium. Arterioscler. Thromb. Vasc. Biol. 1997, 17:2793-2800.
19. Hariawala M.D., Horowitz J.R., Esakof D., Sheriff D.D., Walter D.H., Keyt B., Isner J.M., Symes J.F. VEGF improves myocardial blood flow but produces EDRF-mediated hypotension in porcine hearts. J. Surg. Res. 1996, 63:77-82.
20. Chinen N., Tanihara M., Nakagawa M., Shinozaki K., Yamamoto E., Mizushima Y., Suzuki Y. Action of microparticles of heparin and alginate crosslinked gel when used as injectable artificial matrices to stabilize basic fibroblast growth factor and induce angiogenesis by controlling its release. J. Biomed. Mater. Res. A 2003, 67:61-68.
21. Edelman E.R., Mathiowitz E., Langer R., Klagsbrun M. Controlled and modulated release of basic fibroblast growth factor. Biomaterials 1991, 12:619-626.
22. Harada K., Grossman W., Friedman M., Edelman E.R., Prasad P.V., Keighley C.S., Manning W.J., Sellke F.W., Simons M. Basic fibroblast growth factor improves myocardial function in chronically ischemic porcine hearts. J. Clin. Invest. 1994, 94:623-630.
23. Lopez J.J., Edelman E.R., Stamler A., Hibberd M.G., Prasad P., Caputo R.P., Carrozza J.P., Douglas P.S., Sellke F.W., Simons M. Basic fibroblast growth factor in a porcine model of chronic myocardial ischemia: a comparison of angiographic, echocardiographic and coronary flow parameters. J. Pharmacol. Exp. Ther. 1997, 282:385-390.
24. Laham RJ R.J., Sellke F.W., Edelman E.R., Pearlman J.D., Ware J.A., Brown D.L., Gold J.P., Simons M. 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 1999, 100:1865-1871.
25. Ruvinov E., Leor J., Cohen S. The effects of controlled HGF delivery from an affinity-binding alginate biomaterial on angiogenesis and blood perfusion in a hindlimb ischemia model. Biomaterials 2010, 31:4573-4582.
26. Hao X., Silva E.A., Månsson-Broberg A., Grinnemo K.H., Siddiqui A.J., Dellgren G., Wärdell E., Brodin L.A., Mooney D.J., Sylvén C. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc. Res. 2007, 75:178-185.
27. Fraser J.R., Laurent T.C., Laurent U.B. Hyaluronan: its nature, distribution, functions and turnover. J. Intern. Med. 1997, 242:27-33.
28. Rooney P., Kumar S., Ponting J., Wang M. The role of hyaluronan in tumour neovascularization. Int. J. Cancer 1995, 60:632-636.
29. West D.C., Kumar S. The effect of hyaluronate and its oligosaccharides on endothelial cell proliferation and monolayer integrity. Exp. Cell Res. 1989, 185:179-196.
30. Sattar A., Rooney P., Kumar S., Pye D., West D.C., Scott I., Ledger P. Application of angiogenic oligosaccharides of hyaluronan increases blood vessel numbers in rat skin. J. Invest. Dermatol. 1994, 103:576-579.
31. Riley C.M., Fuegy P.W., Firpo M.A., Shu X.Z., Prestwich G.D., Peattie R.A. Stimulation of in vivo angiogenesis using dual growth factor-loaded crosslinked glycosaminoglycan hydrogels. Biomaterials 2006, 27:5935-5943.
32. Pike D.B., Cai S., Pomraning K.R., Firpo M.A., Fisher R.J., Shu X.Z., Prestwich G.D., Peattie R.A. Heparin-regulated release of growth factors in vitro and angiogenic response in vivo to implanted hyaluronan hydrogels containing VEGF and bFGF. Biomaterials 2006, 27:5242-5251.
33. Peattie R.A., Rieke E.R., Hewett E.M., Fisher R.J., Shu X.Z., Prestwich G.D. Dual growth factor-induced angiogenesis in vivo using hyaluronan hydrogel implants. Biomaterials 2006, 27:1868-1875.
34. Hosack L.W., Firpo M.A., Scott J.A., Prestwich G.D., Peattie R.A. Microvascular maturity elicited in tissue treated with cytokine-loaded hyaluronan-based hydrogels. Biomaterials 2008, 29:2336-2347.
35. Gospodarowicz D., Cheng J. Heparin protects basic and acidic FGF from inactivation. J. Cell. Physiol. 1986, 128:475-484.
36. Folkman J., Shing Y. Control of angiogenesis by heparin and other sulfated polysaccharides. Adv. Exp. Med. Biol. 1992, 313:355-364.
37. Ono K., Saito Y., Yura H., Ishikawa K., Kurita A., Akaike T., Ishihara M. Photocrosslinkable chitosan as a biological adhesive. J. Biomed. Mater. Res. 2000, 49:289-295.
38. Obara K., Ishihara M., Fujita M., Kanatani Y., Hattori H., Matsui T., Takase B., Ozeki Y., Nakamura S., Ishizuka T., Tominaga S., Hiroi S., Kawai T., Maehara T. Acceleration of wound healing in healing-impaired db/db mice with a photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2. Wound Repair Regen. 2005, 13:390-397.
39. Fujita M., Ishihara M., Morimoto Y., Simizu M., Saito Y., Yura H., Matsui T., Takase B., Hattori H., Kanatani Y., Kikuchi M., Maehara T. Efficacy of photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2 in a rabbit model of chronic myocardial infarction. J. Surg. Res. 2005, 126:27-33.
40. Yeo Y., Geng W., Ito T., Kohane D.S., Burdick J.A., Radisic M. Photocrosslinkable hydrogel for myocyte cell culture and injection. J. Biomed. Mater. Res. B Appl. Biomater. 2007, 81:312-322.
41. van Hinsbergh V.W., Collen A., Koolwijk P. Role of fibrin matrix in angiogenesis. Ann. N. Y. Acad. Sci. 2001, 936:426-437.
42. Amrani D.L., Diorio J.P., Delmotte Y. Wound healing. Role of commercial fibrin sealants. Ann. N. Y. Acad. Sci. 2001, 936:566-579.
43. Christman K.L., Vardanian A.J., Fang Q., Sievers R.E., Fok H.H., Lee R.J. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J. Am. Coll. Cardiol. 2004, 44:654-660.
44. Fan C.L., Gao P.J., Gu Y.J., Tang X.F., Liu J.J., Wei J., Inoue K., Zhu D.L. Therapeutic angiogenesis by intramuscular injection of fibrin particles into ischaemic hindlimbs. Clin. Exp. Pharmacol. Physiol. 2006, 33:617-622.
45. Chekanov V.S., Rayel R., Nikolaychik V., Kipshidze N., Baibekov I., Karakozov P., Bajwa T., Akhtar M. Direct fibrin injection to promote new collateral growth in hind limb ischemia in a rabbit model. J. Card. Surg. 2002, 17:502-511.
46. Wong C., Inman E., Spaethe R., Helgerson S. Fibrin-based biomaterials to deliver human growth factors. Thromb. Haemost. 2003, 89:573-582.
47. Fasol R., Schumacher B., Schlaudraff K., Hauenstein K.H., Seitelberger R. Experimental use of a modified fibrin glue to induce site-directed angiogenesis from the aorta to the heart. J. Thorac. Cardiovasc. Surg. 1994, 107:1432-1439.
48. Albes J.M., Klenzner T., Kotzerke J., Thiedemann K.U., Schäfers H.J., Borst H.G. Improvement of tracheal autograft revascularization by means of fibroblast growth factor. Ann. Thorac. Surg. 1994, 57:444-449.
49. Kipshidze N., Kipiani K., Beridze N., Roubin G., Tsapenko M., Shehzad M.Z., Moses J., Kipshidze N.N. Therapeutic angiogenesis for patients with limb ischemia by utilization of fibrin meshwork. Pilot randomized controlled study. Int. Angiol. 2003, 22:349-355.
50. Shireman P.K., Hampton B., Burgess W.H., Greisler H.P. Modulation of vascular cell growth kinetics by local cytokine delivery from fibrin glue suspensions. J. Vasc. Surg. 1999, 29:852-861.
51. Zisch A.H., Schenk U., Schense J.C., Sakiyama-Elbert S.E., Hubbell J.A. Covalently conjugated VEGF-fibrin matrices for endothelialization. J. Control. Release 2001, 72:101-113.
52. Schense J.C., Hubbell J.A. Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa. Bioconjug. Chem. 1999, 10:75-81.
53. Ehrbar M., Zeisberger S.M., Raeber G.P., Hubbell J.A., Schnell C., Zisch A.H. The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis. Biomaterials 2008, 29:1720-1729.
54. Ehrbar M., Djonov V.G., Schnell C., Tschanz S.A., Martiny-Baron G., Schenk U., Wood J., Burri P.H., Hubbell J.A., Zisch A.H. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ. Res. 2004, 94:1124-1132.
55. Ng Y.S., D'Amore P.A. Therapeutic angiogenesis for cardiovascular disease. Curr. Control. Trials Cardiovasc. Med. 2001, 2:278-285.
56. Sakiyama-Elbert S.E., Hubbell J.A. Development of fibrin derivatives for controlled release of heparin-binding growth factors. J. Control. Release 2000, 65:389-402.
57. Yang H.S., Bhang S.H., Hwang J.W., Kim D.I., Kim B.S. Delivery of basic fibroblast growth factor using heparin-conjugated fibrin for therapeutic angiogenesis. Tissue Eng. Part A 2010, 16:2113-2119.
58. Sacchi V., Mittermayr R., Hartinger J., Martino M.M., Lorentz K.M., Wolbank S., Hofmann A., Largo R.A., Marschall J.S., Groppa E., Gianni-Barrera R., Ehrbar M., Hubbell J.A., Redl H., Banfi A. Long-lasting fibrin matrices ensure stable and functional angiogenesis by highly tunable, sustained delivery of recombinant VEGF164. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:6952-6957.
59. Knop K., Hoogenboom R., Fischer D., Schubert U.S. Poly(ethylene glycol) in drug delivery: pros and cons as well as potential alternatives. Angew. Chem. Int. Ed. Engl. 2010, 49:6288-6308.
60. Gentile P., Chiono V., Carmagnola I., Hatton P.V. An overview of poly(lactic-co-glycolic) acid (PLGA)-based biomaterials for bone tissue engineering. Int. J. Mol. Sci. 2014, 15:3640-3659.
61. Almany L., Seliktar D. Biosynthetic hydrogel scaffolds made from fibrinogen and polyethylene glycol for 3D cell cultures. Biomaterials 2005, 26:2467-2477.
62. Rufaihah A.J., Vaibavi S.R., Plotkin M., Shen J., Nithya V., Wang J., Seliktar D., Kofidis T. Enhanced infarct stabilization and neovascularization mediated by VEGF-loaded PEGylated fibrinogen hydrogel in a rodent myocardial infarction model. Biomaterials 2013, 34:8195-8202.
63. Zisch A.H., Lutolf M.P., Ehrbar M., Raeber G.P., Rizzi S.C., Davies N., Schmökel H., Bezuidenhout D., Djonov V., Zilla P., Hubbell J.A. Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth. FASEB J. 2003, 17:2260-2262.
64. Seliktar D., Zisch A.H., Lutolf M.P., Wrana J.L., Hubbell J.A. MMP-2 sensitive, VEGF-bearing bioactive hydrogels for promotion of vascular healing. J. Biomed. Mater. Res. A 2004, 68:704-716.
65. Saik J.E., Gould D.J., Watkins E.M., Dickinson M.E., West J.L. Covalently immobilized platelet-derived growth factor-BB promotes angiogenesis in biomimetic poly(ethylene glycol) hydrogels. Acta Biomater. 2011, 7:133-143.
66. Leslie-Barbick J.E., Saik J.E., Gould D.J., Dickinson M.E., West J.L. The promotion of microvasculature formation in poly(ethylene glycol) diacrylate hydrogels by an immobilized VEGF-mimetic peptide. Biomaterials 2011, 32:5782-5789.
67. Sheridan M.H., Shea L.D., Peters M.C., Mooney D.J. Bioabsorbable polymer scaffolds for tissue engineering capable of sustained growth factor delivery. J. Control. Release 2000, 64:91-102.
68. Peters M.C., Polverini P.J., Mooney D.J. Engineering vascular networks in porous polymer matrices. J. Biomed. Mater. Res. 2002, 60:668-678.
69. Sun Q., Chen R.R., Shen Y., Mooney D.J., Rajagopalan S., Grossman P.M. Sustained vascular endothelial growth factor delivery enhances angiogenesis and perfusion in ischemic hind limb. Pharm. Res. 2005, 22:1110-1116.
70. Richardson T.P., Peters M.C., Ennett A.B., Mooney D.J. Polymeric system for dual growth factor delivery. Nat. Biotechnol. 2001, 19:1029-1034.
71. Martino M.M., Briquez P.S., Güç E., Tortelli F., Kilarski W.W., Metzger S., Rice J.J., Kuhn G.A., Müller R., Swartz M.A., Hubbell J.A. Growth factors engineered for super-affinity to the extracellular matrix enhance tissue healing. Science 2014, 343:885-888.
72. Seliktar D. Designing cell-compatible hydrogels for biomedical applications. Science 2012, 336:1124-1128.
73. Auxenfans C., Lequeux C., Perrusel E., Mojallal A., Kinikoglu B., Damour O. Adipose-derived stem cells (ASCs) as a source of endothelial cells in the reconstruction of endothelialized skin equivalents. J. Tissue Eng. Regen. Med. 2012, 6:512-518.
74. Reagan J., Foo T., Tracy Watson J., Jin W., Moed B.R., Zhang Z. Distinct phenotypes and regenerative potentials of early endothelial progenitor cells and outgrowth endothelial progenitor cells derived from umbilical cord blood. J. Tissue Eng. Regen. Med. 2011, 5:620-628.
75. Asahara T., Masuda H., Takahashi T., Kalka C., Pastore C., Silver M., Kearne M., Magner M., Isner J.M. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 1999, 85:221-228.
76. Pittenger M.F., Martin B.J. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ. Res. 2004, 95:9-20.
77. Minguell J.J., Erices A. Mesenchymal stem cells and the treatment of cardiac disease. Exp. Biol. Med. 2006, 231:39-49.
78. Antonitsis P., Ioannidou-Papagiannaki E., Kaidoglou A., Charokopos N., Kalogeridis A., Kouzi-Koliakou K., Kyriakopoulou I., Klonizakis I., Papakonstantinou C. Cardiomyogenic potential of human adult bone marrow mesenchymal stem cells in vitro. Thorac. Cardiovasc. Surg. 2008, 56:77-82.
79. Zhang X., Wang H., Ma X., Adila A., Wang B., Liu F., Chen B., Wang C., Ma Y. Preservation of the cardiac function in infarcted rat hearts by the transplantation of adipose-derived stem cells with injectable fibrin scaffolds. Exp. Biol. Med. 2010, 235:1505-1515.
80. Chung E., Rytlewski J.A., Merchant A.G., Dhada K.S., Lewis E.W., Suggs L.J. Fibrin-based 3D matrices induce angiogenic behavior of adipose-derived stem cells. Acta Biomater. 2015, 17:78-80.
81. Martens T.P., Godier A.F., Parks J.J., Wan L.Q., Koeckert M.S., Eng G.M., Hudson B.I., Sherman W., Vunjak-Novakovic G. Percutaneous cell delivery into the heart using hydrogels polymerizing in situ. Cell Transplant. 2009, 18:297-304.
82. Barsotti M.C., Magera A., Armani C., Chiellini F., Felice F., Dinucci D., Piras A.M., Minnocci A., Solaro R., Soldani G., Balbarini A., Di Stefano R. Fibrin acts as biomimetic niche inducing both differentiation and stem cell marker expression of early human endothelial progenitor cells. Cell Prolif. 2011, 44:33-48.
83. Bayless K.J., Salazar R., Davis G.E. GE, RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the alpha(v)beta(3) and alpha(5)beta(1) integrins. Am. J. Pathol. 2000, 156:1673-1683.
84. Yu J., Du K.T., Fang Q., Gu Y., Mihardja S.S., Sievers R.E., Wu J.C., Lee R.J. The use of human mesenchymal stem cells encapsulated in RGD modified alginate microspheres in the repair of myocardial infarction in the rat. Biomaterials 2010, 31:7012-7020.
85. Cortes-Morichetti M., Frati G., Schussler O., Duong Van Huyen J.P., Lauret E., Genovese J.A., Carpentier A.F., Chachques J.C. Association between a cell-seeded collagen matrix and cellular cardiomyoplasty for myocardial support and regeneration. Tissue Eng. 2007, 13:2681-2687.
86. Simpson D., Liu H., Fan T.H., Nerem R., Dudley S.C. A tissue engineering approach to progenitor cell delivery results in significant cell engraftment and improved myocardial remodeling. Stem Cells 2007, 25:2350-2357.
87. Simpson D.L., Dudley S.C. Modulation of human mesenchymal stem cell function in a three-dimensional matrix promotes attenuation of adverse remodelling after myocardial infarction. J. Tissue Eng. Regen. Med. 2013, 7:192-202.
88. Genasetti A., Vigetti D., Viola M., Karousou E., Moretto P., Rizzi M., Bartolini B., Clerici M., Pallotti F., De Luca G., Passi A. Hyaluronan and human endothelial cell behavior. Connect. Tissue Res. 2008, 49:120-123.
89. Yee D., Hanjaya-Putra D., Bose V., Luong E., Gerecht S. Hyaluronic acid hydrogels support cord-like structures from endothelial colony-forming cells. Tissue Eng. Part A 2011, 17:1351-1361.
90. Ratliff B.B., Ghaly T., Brudnicki P., Yasuda K., Rajdev M., Bank M., Mares J., Hatzopoulos A.K., Goligorsky M.S. Endothelial progenitors encapsulated in bioartificial niches are insulated from systemic cytotoxicity and are angiogenesis competent. Am. J. Physiol. Ren. Physiol. 2010, 299:F178-F186.
91. Hanjaya-Putra D., Bose V., Shen Y.I., Yee J., Khetan S., Fox-Talbot K., Steenbergen C., Burdick J.A., Gerecht S. Controlled activation of morphogenesis to generate a functional human microvasculature in a synthetic matrix. Blood 2011, 118:804-815.
92. Moon J.J., Saik J.E., Poché R.A., Leslie-Barbick J.E., Lee S.H., Smith A.A., Dickinson M.E., West J.L. Biomimetic hydrogels with pro-angiogenic properties. Biomaterials 2010, 31:3840-3847.
93. Zhang G., Wang X., Wang Z., Zhang J., Suggs L. A PEGylated fibrin patch for mesenchymal stem cell delivery. Tissue Eng. 2006, 12:9-19.
94. Chwalek K., Tsurkan M.V., Freudenberg U., Werner C. Glycosaminoglycan-based hydrogels to modulate heterocellular communication in in vitro angiogenesis models. Sci. Rep. 2014, 4:4414.
95. Prokoph S., Chavakis E., Levental K.R., Zieris A., Freudenberg U., Dimmeler S., Werner C. Sustained delivery of SDF-1α from heparin-based hydrogels to attract circulating pro-angiogenic cells. Biomaterials 2012, 33:4792-4800.
96. Mironi-Harpaz I., Hazanov L., Engel G., Yelin D., Seliktar D. In-situ architectures designed in 3D cell-laden hydrogels using microscopic laser photolithography. Adv. Mater. 2015, 27:1933-1938.
97. Williams D.F. Essential Biomaterials Science 2014, Cambridge University Press, Cambridge, United Kingdom, (381).