Vascularization strategies of engineered tissues and their application in cardiac regeneration

Advanced Drug Delivery Reviews

Volumn 96, Issue , 2016, Pages 183-194

  Sun, Xuetao ^a   Altalhi, Wafa ^a,c   Nunes, Sara S ^a,b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Angiogenesis; Cardiac regeneration; Cardiomyocytes; Endothelial cells; Stem cells; Tissue engineering; Vascularization; Vessels

Indexed keywords

BIOLOGICAL MATERIALS; BIOMATERIALS; CELL ENGINEERING; CELLS; COMPLEX NETWORKS; CYTOLOGY; ENDOTHELIAL CELLS; HISTOLOGY; MICROCIRCULATION; SCAFFOLDS (BIOLOGY); STEM CELLS; TISSUE; TISSUE ENGINEERING;

ANGIOGENESIS; CARDIAC REGENERATION; CARDIOMYOCYTES; VASCULARIZATION; VESSELS;

TISSUE REGENERATION;

ANGIOGENIC FACTOR; ARGINYLGLYCYLASPARTYLSERINE; BIOMATERIAL; COLLAGEN; FIBRIN; FIBRONECTIN; GREEN FLUORESCENT PROTEIN; HYALURONIC ACID; MACROGOL DIACRYLATE; MATRIGEL; POLYGLACTIN; POLYGLYCOLIC ACID; POLYLACTIC ACID; POLYMER; THYMOSIN BETA4; TROPONIN T; UNCLASSIFIED DRUG;

ADIPOSE DERIVED STEM CELL; BLOOD VESSEL GRAFT; BLOOD VESSEL TRANSPLANTATION; CELL CULTURE; CELL PROLIFERATION; COCULTURE; CORONARY ARTERY BYPASS SURGERY; CORONARY ARTERY DISEASE; EMBRYONIC STEM CELL; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; FIBROBLAST CULTURE; HEART; HEART GRAFT; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART REGENERATION; HUMAN; HYDROGEL; INFERIOR CAVA VEIN; MAMMARY ARTERY; MESENCHYMAL STEM CELL; MICROVASCULATURE; MUSCLE STEM CELL; NONHUMAN; PERICYTE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGENERATIVE MEDICINE; REVIEW; SMOOTH MUSCLE FIBER; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE REPAIR; TISSUE SCAFFOLD; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR RING; VASCULARIZATION; ANGIOGENESIS; ANIMAL; BIOPROSTHESIS; BLOOD VESSEL PROSTHESIS; CARDIAC MUSCLE CELL; CHEMISTRY; CYTOLOGY; MICROCIRCULATION; PHYSIOLOGY; PROCEDURES; REGENERATION; STEM CELL;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOPROSTHESIS; BLOOD VESSEL PROSTHESIS; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; HEART; HUMANS; MICROCIRCULATION; MICROVESSELS; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; REGENERATION; STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84951847196     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2015.06.001     Document Type: Review

References (126)

1. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146(6):873-887.
2. Fish J.E., Wythe J.D. The molecular regulation of arteriovenous specification and maintenance. Dev. Dyn. 2015, 244(3):391-409.
3. Bauer S.M., Bauer R.J., Velazquez O.C. Angiogenesis, vasculogenesis, and induction of healing in chronic wounds. Vasc. Endovasc. Surg. 2005, 39(4):293-306.
4. Park K.M., Gerecht S. Harnessing developmental processes for vascular engineering and regeneration. Development 2014, 141(14):2760-2769.
5. Carmeliet P. Angiogenesis in health and disease. Nat. Med. 2003, 9(6):653-660.
6. LeBlanc A.J., et al. Microvascular repair: post-angiogenesis vascular dynamics. Microcirculation 2012, 19(8):676-695.
7. Staiculescu M.C., et al. The role of reactive oxygen species in microvascular remodeling. Int. J. Mol. Sci. 2014, 15(12):23792-23835.
8. Wanjare M., Kusuma S., Gerecht S. Perivascular cells in blood vessel regeneration. Biotechnol. J. 2013, 8(4):434-447.
9. Senger D.R., Davis G.E. Angiogenesis. Cold Spring Harb. Perspect. Biol. 2011, 3(8):a005090.
10. Phng L.K., Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev. Cell 2009, 16(2):196-208.
11. Gaengel K., et al. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2009, 29(5):630-638.
12. Foo S.S., et al. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 2006, 124(1):161-173.
13. Xin M., Olson E.N., Bassel-Duby R. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat. Rev. Mol. Cell Biol. 2013, 14(8):529-541.
14. Fischbach C., Mooney D.J. Polymers for pro- and anti-angiogenic therapy. Biomaterials 2007, 28(12):2069-2076.
15. Phelps E.A., Garcia A.J. Update on therapeutic vascularization strategies. Regen. Med. 2009, 4(1):65-80.
16. Sun X., Nunes S.S. Overview of hydrogel-based strategies for application in cardiac tissue regeneration. Biomed. Mater 2015, 10(3):034005. 10.1088/1748-6041/10/3/034005.
17. Chalupowicz D.G., et al. Fibrin II induces endothelial cell capillary tube formation. J. Cell Biol. 1995, 130(1):207-215.
18. Montesano R., Orci L., Vassalli P. In vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J. Cell Biol. 1983, 97(5 Pt 1):1648-1652.
19. Montesano R., Mouron P., Orci L. Vascular outgrowths from tissue explants embedded in fibrin or collagen gels: a simple in vitro model of angiogenesis. Cell Biol. Int. Rep. 1985, 9(10):869-875.
20. Montesano R., et al. Basic fibroblast growth factor induces angiogenesis in vitro. Proc. Natl. Acad. Sci. U. S. A. 1986, 83(19):7297-7301.
21. Hoying J.B., Boswell C.A., Williams S.K. Angiogenic potential of microvessel fragments established in three-dimensional collagen gels. In Vitro Cell. Dev. Biol. Anim. 1996, 32(7):409-419.
22. Hoying J.B., Williams S.K. Effects of basic fibroblast growth factor on human microvessel endothelial cell migration on collagen I correlates inversely with adhesion and is cell density dependent. J. Cell. Physiol. 1996, 168(2):294-304.
23. Ingber D.E., Folkman J. Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J. Cell Biol. 1989, 109(1):317-330.
24. Montesano R., et al. Phorbol ester induces cultured endothelial cells to invade a fibrin matrix in the presence of fibrinolytic inhibitors. J. Cell. Physiol. 1987, 132(3):509-516.
25. Kubota Y., et al. Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J. Cell Biol. 1988, 107(4):1589-1598.
26. Nehls V., Drenckhahn D. A novel, microcarrier-based in vitro assay for rapid and reliable quantification of three-dimensional cell migration and angiogenesis. Microvasc. Res. 1995, 50(3):311-322.
27. Nunes S.S., et al. Syndecan-4 contributes to endothelial tubulogenesis through interactions with two motifs inside the pro-angiogenic N-terminal domain of thrombospondin-1. J. Cell. Physiol. 2008, 214(3):828-837.
28. Yee D., et al. Hyaluronic acid hydrogels support cord-like structures from endothelial colony-forming cells. Tissue Eng. Part A 2011, 17(9-10):1351-1361.
29. Moon J.J., et al. Micropatterning of poly(ethylene glycol) diacrylate hydrogels with biomolecules to regulate and guide endothelial morphogenesis. Tissue Eng. Part A 2009, 15(3):579-585.
30. Hanjaya-Putra D., et al. Controlled activation of morphogenesis to generate a functional human microvasculature in a synthetic matrix. Blood 2011, 118(3):804-815.
31. Geevarghese A., Herman I.M. Pericyte-endothelial crosstalk: implications and opportunities for advanced cellular therapies. Transl. Res. 2014, 163(4):296-306.
32. Nehls V., Drenckhahn D. A microcarrier-based cocultivation system for the investigation of factors and cells involved in angiogenesis in three-dimensional fibrin matrices in vitro. Histochem. Cell Biol. 1995, 104(6):459-466.
33. Stratman A.N., et al. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 2009, 114(24):5091-5101.
34. Schechner J.S., et al. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(16):9191-9196.
35. Enis D.R., et al. Induction, differentiation, and remodeling of blood vessels after transplantation of Bcl-2-transduced endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(2):425-430.
36. Shepherd B.R., et al. Human aortic smooth muscle cells promote arteriole formation by coengrafted endothelial cells. Tissue Eng. Part A 2009, 15(1):165-173.
37. Waters J.P., et al. In vitro self-assembly of human pericyte-supported endothelial microvessels in three-dimensional coculture: a simple model for interrogating endothelial-pericyte interactions. J. Vasc. Res. 2013, 50(4):324-331.
38. Kusuma S., et al. Self-organized vascular networks from human pluripotent stem cells in a synthetic matrix. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(31):12601-12606.
39. Koike N., et al. Tissue engineering: creation of long-lasting blood vessels. Nature 2004, 428(6979):138-139.
40. Yuan F., et al. Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res. 1994, 54(17):4564-4568.
41. Tsigkou O., et al. Engineered vascularized bone grafts. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(8):3311-3316.
42. Boyd N.L., et al. Microvascular mural cell functionality of human embryonic stem cell-derived mesenchymal cells. Tissue Eng. Part A 2011, 17(11-12):1537-1548.
43. Boyd N.L., et al. Dissecting the role of human embryonic stem cell-derived mesenchymal cells in human umbilical vein endothelial cell network stabilization in three-dimensional environments. Tissue Eng. Part A 2013, 19(1-2):211-223.
44. Chen Y.C., et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv. Funct. Mater. 2012, 22(10):2027-2039.
45. Rao R.R., et al. Matrix composition regulates three-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 2012, 15(2):253-264.
46. Samuel R., et al. Generation of functionally competent and durable engineered blood vessels from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(31):12774-12779.
47. Montesano R., Pepper M.S., Orci L. Paracrine induction of angiogenesis in vitro by Swiss 3T3 fibroblasts. J. Cell Sci. 1993, 105(Pt 4):1013-1024.
48. Bishop E.T., et al. An in vitro model of angiogenesis: basic features. Angiogenesis 1999, 3(4):335-344.
49. Black A.F., et al. In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J. 1998, 12(13):1331-1340.
50. Hudon V., et al. A tissue-engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary-like tube formation in vitro. Br. J. Dermatol. 2003, 148(6):1094-1104.
51. Rochon M.H., et al. Normal human epithelial cells regulate the size and morphology of tissue-engineered capillaries. Tissue Eng. Part A 2010, 16(5):1457-1468.
52. Levenberg S., et al. Engineering vascularized skeletal muscle tissue. Nat. Biotechnol. 2005, 23(7):879-884.
53. Nicosia R.F., Ottinetti A. Growth of microvessels in serum-free matrix culture of rat aorta. A quantitative assay of angiogenesis in vitro. Lab. Investig. 1990, 63(1):115-122.
54. Masson V.V., et al. Mouse aortic ring assay: a new approach of the molecular genetics of angiogenesis. Biol. Proced. Online 2002, 4:24-31.
55. Zhu W.H., et al. The mouse aorta model: influence of genetic background and aging on bFGF- and VEGF-induced angiogenic sprouting. Angiogenesis 2003, 6(3):193-199.
56. Stiffey-Wilusz J., et al. An ex vivo angiogenesis assay utilizing commercial porcine carotid artery: modification of the rat aortic ring assay. Angiogenesis 2001, 4(1):3-9.
57. Baker M., et al. Use of the mouse aortic ring assay to study angiogenesis. Nat. Protoc. 2012, 7(1):89-104.
58. Chiu L.L., et al. Perfusable branching microvessel bed for vascularization of engineered tissues. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(50):E3414-E3423.
59. Nunes S.S., et al. Angiogenic potential of microvessel fragments is independent of the tissue of origin and can be influenced by the cellular composition of the implants. Microcirculation 2010, 17(7):557-567.
60. Nunes S.S., et al. Implanted microvessels progress through distinct neovascularization phenotypes. Microvasc. Res. 2010, 79(1):10-20.
61. Shepherd B.R., et al. Rapid perfusion and network remodeling in a microvascular construct after implantation. Arterioscler. Thromb. Vasc. Biol. 2004, 24(5):898-904.
62. Nunes S.S., et al. Vessel arterial-venous plasticity in adult neovascularization. PLoS One 2011, 6(11):e27332.
63. Nunes S.S., et al. Generation of a functional liver tissue mimic using adipose stromal vascular fraction cell-derived vasculatures. Sci. Rep. 2013, 3:2141.
64. Pilia M., et al. Transplantation and perfusion of microvascular fragments in a rodent model of volumetric muscle loss injury. Eur. Cell. Mater. 2014, 28:11-23. (discussion 23-4).
65. Hwang J.H., et al. Combination therapy of human adipose-derived stem cells and basic fibroblast growth factor hydrogel in muscle regeneration. Biomaterials 2013, 34(25):6037-6045.
66. Park J.K., et al. Losartan improves adipose tissue-derived stem cell niche by inhibiting transforming growth factor-beta and fibrosis in skeletal muscle injury. Cell Transplant. 2012, 21(11):2407-2424.
67. Ahuja P., Sdek P., MacLellan W.R. Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol. Rev. 2007, 87(2):521-544.
68. Post M.J., Rahimi N., Caolo V. Update on vascularization in tissue engineering. Regen. Med. 2013, 8(6):759-770.
69. Radisic M., et al. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol. Bioeng. 2006, 93(2):332-343.
70. Davis B.H., et al. An in vitro system to evaluate the effects of ischemia on survival of cells used for cell therapy. Ann. Biomed. Eng. 2007, 35(8):1414-1424.
71. Cheema U., et al. Spatially defined oxygen gradients and vascular endothelial growth factor expression in an engineered 3D cell model. Cell. Mol. Life Sci. 2008, 65(1):177-186.
72. Stevens K.R., et al. Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(39):16568-16573.
73. Lesman A., et al. Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng. Part A 2010, 16(1):115-125.
74. Shepherd B.R., Hoying J.B., Williams S.K. Microvascular transplantation after acute myocardial infarction. Tissue Eng. 2007, 13(12):2871-2879.
75. Martinez E.C., et al. Post-ischaemic angiogenic therapy using in vivo prevascularized ascorbic acid-enriched myocardial artificial grafts improves heart function in a rat model. J. Tissue Eng. Regen. Med. 2013, 7(3):203-212.
76. Pagliari S., et al. A multistep procedure to prepare pre-vascularized cardiac tissue constructs using adult stem sells, dynamic cell cultures, and porous scaffolds. Front. Physiol. 2014, 5:210.
77. Thomson K.S., et al. Prevascularized microtemplated fibrin scaffolds for cardiac tissue engineering applications. Tissue Eng. Part A 2013, 19(7-8):967-977.
78. Tulloch N.L., et al. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ. Res. 2011, 109(1):47-59.
79. Radisic M., et al. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(52):18129-18134.
80. Song H., et al. Interrogating functional integration between injected pluripotent stem cell-derived cells and surrogate cardiac tissue. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(8):3329-3334.
81. Shimizu T., et al. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials 2003, 24(13):2309-2316.
82. Sekine H., et al. Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 2008, 118(14 Suppl.):S145-S152.
83. Masumoto H., et al. Human iPS cell-engineered cardiac tissue sheets with cardiomyocytes and vascular cells for cardiac regeneration. Sci. Rep. 2014, 4:6716.
84. Dvir T., et al. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(35):14990-14995.
85. Chong J.J., et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014, 510(7504):273-277.
86. Stewart D.J., et al. VEGF gene therapy fails to improve perfusion of ischemic myocardium in patients with advanced coronary disease: results of the NORTHERN trial. Mol. Ther. 2009, 17(6):1109-1115.
87. Losordo D.W., et al. Gene therapy for myocardial angiogenesis: initial clinical results with direct myocardial injection of phVEGF165 as sole therapy for myocardial ischemia. Circulation 1998, 98(25):2800-2804.
88. Grines C.L., et al. Angiogenic Gene Therapy (AGENT) trial in patients with stable angina pectoris. Circulation 2002, 105(11):1291-1297.
89. Grines C., et al. Angiogenic gene therapy with adenovirus 5 fibroblast growth factor-4 (Ad5FGF-4): a new option for the treatment of coronary artery disease. Am. J. Cardiol. 2003, 92(9B):24N-31N.
90. Henry T.D., et al. Effects of Ad5FGF-4 in patients with angina: an analysis of pooled data from the AGENT-3 and AGENT-4 trials. J. Am. Coll. Cardiol. 2007, 50(11):1038-1046.
91. Rajagopalan S., et al. Use of a constitutively active hypoxia-inducible factor-1alpha transgene as a therapeutic strategy in no-option critical limb ischemia patients: phase I dose-escalation experience. Circulation 2007, 115(10):1234-1243.
92. Powell R.J., et al. Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia. Circulation 2008, 118(1):58-65.
93. Gupta R., Tongers J., Losordo D.W. Human studies of angiogenic gene therapy. Circ. Res. 2009, 105(8):724-736.
94. Valina C., et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur. Heart J. 2007, 28(21):2667-2677.
95. Miyahara Y., et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 2006, 12(4):459-465.
96. Perin E.C., et al. Adipose-derived regenerative cells in patients with ischemic cardiomyopathy: the PRECISE trial. Am. Heart J. 2014, 168(1):88-95. (e2).
97. Houtgraaf J.H., et al. First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. J. Am. Coll. Cardiol. 2012, 59(5):539-540.
98. Losordo D.W., et al. Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circ. Res. 2011, 109(4):428-436.
99. Bolli R., et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011, 378(9806):1847-1857.
100. Chugh A.R., et al. Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 2012, 126(11 Suppl. 1):S54-S64.
101. Beltrami A.P., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003, 114(6):763-776.
102. Hosoda T., et al. Clonality of mouse and human cardiomyogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(40):17169-17174.
103. Murry C.E., et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 2004, 428(6983):664-668.
104. Zaruba M.M., et al. Cardiomyogenic potential of C-kit(+)-expressing cells derived from neonatal and adult mouse hearts. Circulation 2010, 121(18):1992-2000.
105. + precursors support postinfarction myogenesis in the neonatal, but not adult, heart. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(33):13380-13385.
106. Tang X.L., et al. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation 2010, 121(2):293-305.
107. Chimenti I., et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ. Res. 2010, 106(5):971-980.
108. + cells minimally contribute cardiomyocytes to the heart. Nature 2014, 509(7500):337-341.
109. Hesse M., Fleischmann B.K., Kotlikoff M.I. Concise review: the role of C-kit expressing cells in heart repair at the neonatal and adult stage. Stem Cells 2014, 32(7):1701-1712.
110. Taljaard M., et al. Rationale and design of Enhanced Angiogenic Cell Therapy in Acute Myocardial Infarction (ENACT-AMI): the first randomized placebo-controlled trial of enhanced progenitor cell therapy for acute myocardial infarction. Am. Heart J. 2010, 159(3):354-360.
111. Noiseux N., et al. The current state of stem cell therapeutics: Canadian approaches in the international context. Can. J. Cardiol. 2014, 30(11):1361-1369.
112. Laflamme M.A., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 2007, 25(9):1015-1024.
113. Elcin 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(7):558-565.
114. Fournier N., Doillon C.J. Biological molecule-impregnated polyester: an in vivo angiogenesis study. Biomaterials 1996, 17(17):1659-1665.
115. Hendel R.C., et al. Effect of intracoronary recombinant human vascular endothelial growth factor on myocardial perfusion: evidence for a dose-dependent effect. Circulation 2000, 101(2):118-121.
116. Henry T.D., et al. The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation 2003, 107(10):1359-1365.
117. Iwakura A., et al. Intramyocardial sustained delivery of basic fibroblast growth factor improves angiogenesis and ventricular function in a rat infarct model. Heart Vessel. 2003, 18(2):93-99.
118. Perets A., et al. Enhancing the vascularization of three-dimensional porous alginate scaffolds by incorporating controlled release basic fibroblast growth factor microspheres. J. Biomed. Mater. Res. A 2003, 65(4):489-497.
119. Hegen A., et al. Efficient in vivo vascularization of tissue-engineering scaffolds. J. Tissue Eng. Regen. Med. 2011, 5(4):e52-e62.
120. Kaully T., et al. Vascularization-: the conduit to viable engineered tissues. Tissue Eng. Part B Rev. 2009, 15(2):159-169.
121. Krishnan L., et al. Manipulating the microvasculature and its microenvironment. Crit. Rev. Biomed. Eng. 2013, 41(2):91-123.
122. Melero-Martin J.M., et al. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood 2007, 109(11):4761-4768.
123. Robey T.E., et al. Systems approaches to preventing transplanted cell death in cardiac repair. J. Mol. Cell. Cardiol. 2008, 45(4):567-581.
124. Zhang M., et al. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J. Mol. Cell. Cardiol. 2001, 33(5):907-921.
125. Zhu W.Z., et al. Human embryonic stem cells and cardiac repair. Transplant. Rev. (Orlando) 2009, 23(1):53-68.
126. Fernandes S., et al. Human embryonic stem cell-derived cardiomyocytes engraft but do not alter cardiac remodeling after chronic infarction in rats. J. Mol. Cell. Cardiol. 2010, 49(6):941-949.