Controlled protein delivery in the generation of microvascular networks

Drug Delivery and Translational Research

Volumn 5, Issue 2, 2015, Pages 75-88

  Andrejecsk, Jillian W ^a   Chang, William G ^b   Pober, Jordan S ^b   Saltzman, W Mark ^a  

^a Yale University   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Microvascular network; Protein delivery; Stabilization; Tissue engineering; Vascularization

Indexed keywords

ANGIOGENIC PROTEIN; ANGIOPOIETIN; CHEMOKINE; FIBROBLAST GROWTH FACTOR; HYBRID PROTEIN; NANOPARTICLE; PLATELET DERIVED GROWTH FACTOR; POLYMER; PROTEIN; SCAFFOLD PROTEIN; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN; DELAYED RELEASE FORMULATION;

CONTROLLED PROTEIN DELIVERY; DRUG DELIVERY SYSTEM; HUMAN; IMMOBILIZATION; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; REVASCULARIZATION; REVIEW; TISSUE ENGINEERING; VASCULARIZATION; ADMINISTRATION AND DOSAGE; ANGIOGENESIS; ANIMAL; DELAYED RELEASE FORMULATION; DRUG EFFECTS; THERAPEUTIC USE;

ANIMALS; DELAYED-ACTION PREPARATIONS; DRUG DELIVERY SYSTEMS; HUMANS; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEINS;

EID: 84924354156     PISSN: 2190393X     EISSN: 21903948     Source Type: Journal    
DOI: 10.1007/s13346-012-0122-y     Document Type: Review

References (111)

1. Iwasa J, et al. Clinical application of scaffolds for cartilage tissue engineering. Knee Surg Sports Traumatol Arthrosc. 2009;17(6):561–77.
2. Roh JD, et al. Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc Natl Acad Sci U S A. 2010;107(10):4669–74.
3. Patterson JT, et al. Tissue-engineered vascular grafts for use in the treatment of congenital heart disease: from the bench to the clinic and back again. Regen Med. 2012;7(3):409–19.
4. Olausson, M., et al. Transplantation of an allogeneic vein bioengineered with autologous stem cells: a proof-of-concept study. Lancet. 2012;380(9838):230–7.
5. Macchiarini P, et al. Clinical transplantation of a tissue-engineered airway. Lancet. 2008;372(9655):2023–30.
6. Jungebluth P, et al. Tracheobronchial transplantation with a stem-cell-seeded bioartificial nanocomposite: a proof-of-concept study. Lancet. 2011;378(9808):1997–2004.
7. Drewa T, Adamowicz J, Sharma A. Tissue engineering for the oncologic urinary bladder. Nat Rev Urol. 2012;9(10):561–72.
8. Enis DR, 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):425–30.
9. Schechner JS, 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):9191–6.
10. Shepherd BR, et al. Human aortic smooth muscle cells promote arteriole formation by coengrafted endothelial cells. Tissue Eng Part A. 2009;15(1):165–73.
11. Maier CL, et al. Explant outgrowth, propagation and characterization of human pericytes. Microcirculation. 2010;17(5):367–80.
12. Traktuev DO, et al. Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res. 2009;104(12):1410–20.
13. Ford MC, et al. A macroporous hydrogel for the coculture of neural progenitor and endothelial cells to form functional vascular networks in vivo. Proc Natl Acad Sci U S A. 2006;103(8):2512–7.
14. Gerhardt H, Betsholtz C. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res. 2003;314(1):15–23.
15. Gerhardt H, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163–77.
16. Sun Q, et al. Sustained release of multiple growth factors from injectable polymeric system as a novel therapeutic approach towards angiogenesis. Pharm Res. 2010;27(2):264–71.
17. Richardson TP, et al. Polymeric system for dual growth factor delivery. Nat Biotechnol. 2001;19(11):1029–34.
18. Freeman I, Cohen S. The influence of the sequential delivery of angiogenic factors from affinity-binding alginate scaffolds on vascularization. Biomaterials. 2009;30(11):2122–31.
19. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25(4):581–611.
20. Zhang G, Suggs LJ. Matrices and scaffolds for drug delivery in vascular tissue engineering. Adv Drug Deliv Rev. 2007;59(4–5):360–73.
21. Leung DW, et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246(4935):1306–9.
22. Takeshita S, et al. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest. 1994;93(2):662–70.
23. Springer ML, et al. Localized arteriole formation directly adjacent to the site of VEGF-induced angiogenesis in muscle. Mol Ther. 2003;7(4):441–9.
24. Lee RJ, et al. VEGF gene delivery to myocardium: deleterious effects of unregulated expression. Circulation. 2000;102(8):898–901.
25. Ozawa CR, et al. Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis. J Clin Investig. 2004;113(4):516–27.
26. Henry TD, et al. The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation. 2003;107(10):1359–65.
27. Ennett AB, Kaigler D, Mooney DJ. Temporally regulated delivery of VEGF in vitro and in vivo. J Biomed Mater Res A. 2006;79(1):176–84.
28. Rebar EJ, et al. Induction of angiogenesis in a mouse model using engineered transcription factors. Nat Med. 2002;8(12):1427–32.
29. Hao X, et al. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc Res. 2007;75(1):178–85.
30. Murakami M, Simons M. Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol. 2008;15(3):215–20.
31. Javerzat S, Auguste P, Bikfalvi A. The role of fibroblast growth factors in vascular development. Trends Mol Med. 2002;8(10):483–9.
32. Presta M, et al. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 2005;16(2):159–78.
33. Murakami M, et al. FGF-dependent regulation of VEGF receptor 2 expression in mice. J Clin Invest. 2011;121(7):2668–78.
34. Cao R, et al. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med. 2003;9(5):604–13.
35. Nakamura T, et al. Molecular cloning and expression of human hepatocyte growth factor. Nature. 1989;342(6248):440–3.
36. Distler J.H., et al. Angiogenic and angiostatic factors in the molecular control of angiogenesis. The quarterly journal of nuclear medicine: official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology (IAR) 2003;47(3):149–161.
37. Schroder K, et al. Hepatocyte growth factor induces a proangiogenic phenotype and mobilizes endothelial progenitor cells by activating Nox2. Antioxid Redox Signal. 2011;15(4):915–23.
38. Keeley EC, Mehrad B, Strieter RM. Chemokines as mediators of neovascularization. Arterioscler Thromb Vasc Biol. 2008;28(11):1928–36.
39. Addison CL, et al. The CXC chemokine receptor 2, CXCR2, is the putative receptor for ELR+CXC chemokine-induced angiogenic activity. J Immunol. 2000;165(9):5269–77.
40. Murdoch C, Monk PN, Finn A. CXC chemokine receptor expression on human endothelial cells. Cytokine. 1999;11(9):704–12.
41. Hristov M, et al. Importance of CXC chemokine receptor 2 in the homing of human peripheral blood endothelial progenitor cells to sites of arterial injury. Circ Res. 2007;100(4):590–7.
42. Kocher AA, et al. Myocardial homing and neovascularization by human bone marrow angioblasts is regulated by IL-8/Gro CXC chemokines. J Mol Cell Cardiol. 2006;40(4):455–64.
43. Lau TT, Wang DA. Stromal cell-derived factor-1 (SDF-1): homing factor for engineered regenerative medicine. Expert Opin Biol Ther. 2011;11(2):189–97.
44. Stamatovic SM, et al. CCL2 regulates angiogenesis via activation of Ets-1 transcription factor. J Immunol. 2006;177(4):2651–61.
45. Galvez BG, et al. Membrane type 1-matrix metalloproteinase is regulated by chemokines monocyte-chemoattractant protein-1/CCL2 and interleukin-8/CXCL8 in endothelial cells during angiogenesis. J Biol Chem. 2005;280(2):1292–8.
46. Weber KS, et al. Expression of CCR2 by endothelial cells: implications for MCP-1 mediated wound injury repair and In vivo inflammatory activation of endothelium. Arterioscler Thromb Vasc Biol. 1999;19(9):2085–93.
47. Aplin AC, Fogel E, Nicosia RF. MCP-1 promotes mural cell recruitment during angiogenesis in the aortic ring model. Angiogenesis. 2010;13(3):219–26.
48. Barcelos LS, et al. Production and in vivo effects of chemokines CXCL1-3/KC and CCL2/JE in a model of inflammatory angiogenesis in mice. Inflamm Res. 2004;53(10):576–84.
49. Goede V, et al. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int J Cancer. 1999;82(5):765–70.
50. Salcedo R, et al. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood. 2000;96(1):34–40.
51. Jay SM, et al. Dual delivery of VEGF and MCP-1 to support endothelial cell transplantation for therapeutic vascularization. Biomaterials. 2010;31(11):3054–62.
52. Hong KH, Ryu J, Han KH. Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A. Blood. 2005;105(4):1405–7.
53. Salcedo R, et al. Eotaxin (CCL11) induces in vivo angiogenic responses by human CCR3+ endothelial cells. J Immunol. 2001;166(12):7571–8.
54. Strasly M, et al. CCL16 activates an angiogenic program in vascular endothelial cells. Blood. 2004;103(1):40–9.
55. Piao W, et al. Transplantation of Sendai viral angiopoietin-1-modified mesenchymal stem cells for ischemic limb disease. Angiogenesis. 2010;13(3):203–10.
56. Ribatti D, Nico B, Crivellato E. The role of pericytes in angiogenesis. Int J Dev Biol. 2011;55(3):261–8.
57. Lindahl P, et al. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277(5323):242–5.
58. Edelberg JM, et al. PDGF mediates cardiac microvascular communication. J Clin Invest. 1998;102(4):837–43.
59. Bar RS, et al. The effects of platelet-derived growth factor in cultured microvessel endothelial cells. Endocrinology. 1989;124(4):1841–8.
60. Battegay EJ, et al. PDGF-BB modulates endothelial proliferation and angiogenesis in vitro via PDGF beta-receptors. J Cell Biol. 1994;125(4):917–28.
61. Uemura A, et al. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J Clin Invest. 2002;110(11):1619–28.
62. Fukuhara S, et al. Angiopoietin-1/Tie2 receptor signaling in vascular quiescence and angiogenesis. Histol Histopathol. 2010;25(3):387–96.
63. Fukuhara S, et al. Tie2 is tied at the cell–cell contacts and to extracellular matrix by angiopoietin-1. Exp Mol Med. 2009;41(3):133–9.
64. Thomas M, Augustin HG. The role of the angiopoietins in vascular morphogenesis. Angiogenesis. 2009;12(2):125–37.
65. Gale NW, Yancopoulos GD. Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development. Genes Dev. 1999;13(9):1055–66.
66. Brindle NP, Saharinen P, Alitalo K. Signaling and functions of angiopoietin-1 in vascular protection. Circ Res. 2006;98(8):1014–23.
67. Douglas HE. TGF-SS in wound healing: a review. J Wound Care. 2010;19(9):403–6.
68. Wipff PJ, Hinz B. Integrins and the activation of latent transforming growth factor beta1—an intimate relationship. Eur J Cell Biol. 2008;87(8–9):601–15.
69. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000;14(2):163–76.
70. Pepper MS. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 1997;8(1):21–43.
71. Weinstein M, Yang X, Deng C. Functions of mammalian Smad genes as revealed by targeted gene disruption in mice. Cytokine Growth Factor Rev. 2000;11(1–2):49–58.
72. Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9(6):685–93.
73. Chambers RC, et al. Global expression profiling of fibroblast responses to transforming growth factor-beta1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am J Pathol. 2003;162(2):533–46.
74. Antonelli-Orlidge A, et al. An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proc Natl Acad Sci U S A. 1989;86(12):4544–8.
75. Bhang SH, et al. Delivery of fibroblast growth factor 2 enhances the viability of cord blood-derived mesenchymal stem cells transplanted to ischemic limbs. J Biosci Bioeng. 2011;111(5):584–9.
76. Layman H, et al. 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 Part A. 2011;17(1–2):243–54.
77. Madduri S, et al. Collagen nerve conduits releasing the neurotrophic factors GDNF and NGF. J Control Release. 2010;143(2):168–74.
78. Jay SM, et al. Engineering of multifunctional gels integrating highly efficient growth factor delivery with endothelial cell transplantation. FASEB J. 2008;22(8):2949–56.
79. Zisch AH, et al. Engineered fibrin matrices for functional display of cell membrane-bound growth factor-like activities: study of angiogenic signaling by ephrin-B2. Biomaterials. 2004;25(16):3245–57.
80. Ehrbar M, et al. The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis. Biomaterials. 2008;29(11):1720–9.
81. Zisch AH, et al. Covalently conjugated VEGF—fibrin matrices for endothelialization. J Control Release. 2001;72(1–3):101–13.
82. Steffens GC, et al. Modulation of angiogenic potential of collagen matrices by covalent incorporation of heparin and loading with vascular endothelial growth factor. Tissue Eng. 2004;10(9–10):1502–9.
83. Guo HD, et al. Sustained delivery of VEGF from designer self-assembling peptides improves cardiac function after myocardial infarction. Biochem Biophys Res Commun. 2012;424(1):105–11.
84. Zhao W, et al. Human basic fibroblast growth factor fused with Kringle4 peptide binds to a fibrin scaffold and enhances angiogenesis. Tissue Eng Part A. 2009;15(5):991–8.
85. Lin RZ, Melero-Martin JM. Fibroblast growth factor-2 facilitates rapid anastomosis formation between bioengineered human vascular networks and living vasculature. Methods. 2012;56(3):440–51.
86. Kaigler D, Silva EA, Mooney DJ. Guided bone regeneration (GBR) utilizing injectable vascular endothelial growth factor (VEGF) delivery gel. J Periodontol. 2012. doi:10.1902/jop.2012.110684.
87. Hadjipanayi E, et al. Injectable system for spatio-temporally controlled delivery of hypoxia-induced angiogenic signalling. J Control Release. 2012;161(3):852–60.
88. Lin YD, et al. Instructive nanofiber scaffolds with VEGF create a microenvironment for arteriogenesis and cardiac repair. Sci Transl Med. 2012;4(146):146ra109.
89. McQuilling JP, et al. New alginate microcapsule system for angiogenic protein delivery and immunoisolation of islets for transplantation in the rat omentum pouch. Transplant Proc. 2011;43(9):3262–4.
90. Banquet S, et al. Arteriogenic therapy by intramyocardial sustained delivery of a novel growth factor combination prevents chronic heart failure. Circulation. 2011;124(9):1059–69.
91. Kuraitis D, et al. A stromal cell-derived factor-1 releasing matrix enhances the progenitor cell response and blood vessel growth in ischaemic skeletal muscle. Eur Cell Mater. 2011;22:109–23.
92. Nagai N, et al. Preparation and characterization of collagen microspheres for sustained release of VEGF. J Mater Sci Mater Med. 2010;21(6):1891–8.
93. Patel ZS, et al. In vitro and in vivo release of vascular endothelial growth factor from gelatin microparticles and biodegradable composite scaffolds. Pharm Res. 2008;25(10):2370–8.
94. Tan Q, et al. Controlled release of chitosan/heparin nanoparticle-delivered VEGF enhances regeneration of decellularized tissue-engineered scaffolds. Int J Nanomedicine. 2011;6:929–42.
95. Formiga FR, et al. Sustained release of VEGF through PLGA microparticles improves vasculogenesis and tissue remodeling in an acute myocardial ischemia-reperfusion model. J Control Release. 2010;147(1):30–7.
96. Lee J, et al. Active blood vessel formation in the ischemic hindlimb mouse model using a microsphere/hydrogel combination system. Pharm Res. 2010;27(5):767–74.
97. Jeon O, et al. Long-term and zero-order release of basic fibroblast growth factor from heparin-conjugated poly(l-lactide-co-glycolide) nanospheres and fibrin gel. Biomaterials. 2006;27(8):1598–607.
98. King TW, Patrick Jr CW. Development and in vitro characterization of vascular endothelial growth factor (VEGF)-loaded poly(dl-lactic-co-glycolic acid)/poly(ethylene glycol) microspheres using a solid encapsulation/single emulsion/solvent extraction technique. J Biomed Mater Res. 2000;51(3):383–90.
99. Elbjeirami WM, West JL. Angiogenesis-like activity of endothelial cells co-cultured with VEGF-producing smooth muscle cells. Tissue Eng. 2006;12(2):381–90.
100. Zhu K., et al. Novel vascular endothelial growth factor gene delivery system-manipulated mesenchymal stem cells repair infarcted myocardium. Exp Biol Med (Maywood). 2012;237(6):678–87.
101. Levenberg S, et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol. 2005;23(7):879–84.
102. Springer ML, et al. Induction of angiogenesis by implantation of encapsulated primary myoblasts expressing vascular endothelial growth factor. J Gene Med. 2000;2(4):279–88.
103. Koike N, et al. Tissue engineering: creation of long-lasting blood vessels. Nature. 2004;428(6979):138–9.
104. Soppimath KS, et al. Stimulus-responsive “smart” hydrogels as novel drug delivery systems. Drug Dev Ind Pharm. 2002;28(8):957–74.
105. Hoare T, et al. Magnetically triggered nanocomposite membranes: a versatile platform for triggered drug release. Nano Lett. 2011;11(3):1395–400.
106. Hawkins AM, Satarkar NS, Hilt JZ. Nanocomposite degradable hydrogels: demonstration of remote controlled degradation and drug release. Pharm Res. 2009;26(3):667–73.
107. Lee H, et al. Local delivery of basic fibroblast growth factor increases both angiogenesis and engraftment of hepatocytes in tissue-engineered polymer devices. Transplantation. 2002;73(10):1589–93.
108. Kedem A, et al. Vascular endothelial growth factor-releasing scaffolds enhance vascularization and engraftment of hepatocytes transplanted on liver lobes. Tissue Eng. 2005;11(5–6):715–22.
109. Chen L, et al. Loading of VEGF to the heparin cross-linked demineralized bone matrix improves vascularization of the scaffold. J Mater Sci Mater Med. 2010;21(1):309–17.
110. Kanczler JM, et al. The effect of the delivery of vascular endothelial growth factor and bone morphogenic protein-2 to osteoprogenitor cell populations on bone formation. Biomaterials. 2010;31(6):1242–50.
111. Kelpke SS, et al. Site-specific delivery of acidic fibroblast growth factor stimulates angiogenic and osteogenic responses in vivo. J Biomed Mater Res A. 2004;71(2):316–25.