Spatiotemporal control over growth factor signaling for therapeutic neovascularization

Advanced Drug Delivery Reviews

Volumn 59, Issue 13, 2007, Pages 1340-1350

  Cao, Lan ^a   Mooney, David J ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Angiogenesis; Delivery system; Growth factor; Quantitative; Temporal and spatial; Therapeutic neovascularization

Indexed keywords

CELL GROWTH; MATHEMATICAL MODELS; TISSUE ENGINEERING;

ANGIOGENESIS; DELIVERY SYSTEM; THERAPEUTIC NEOVASCULARIZATION;

DRUG THERAPY;

ADENOVIRUS VECTOR; ANGIOPOIETIN 1; ANGIOPOIETIN 2; FIBROBLAST GROWTH FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACENTAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; SCATTER FACTOR; SOMATOMEDIN; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; DRUG DELIVERY SYSTEM; ENDOTHELIUM CELL; HYDROGEL; IMAGING; ISOTOPE LABELING; KNOCKOUT MOUSE; MATHEMATICAL MODEL; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, STATISTICAL; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; TISSUE ENGINEERING;

EID: 36049046711     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2007.08.012     Document Type: Review

References (159)

1. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 438 (2005) 932-936
2. Ferrara N., and Kerbel R.S. Angiogenesis as a therapeutic target. Nature 438 (2005) 967-974
3. Folkman J. Diagnostic and therapeutic applications of angiogenesis research. C. R. Acad. Sci., Ser. III 316 (1993) 909-918
4. Isner J.M. Therapeutic angiogenesis: a new frontier for vascular therapy. Vasc. Med. 1 (1996) 79-87
5. Hughes G.C., and Annex B.H. Angiogenic therapy for coronary artery and peripheral arterial disease. Expert Rev. Cardiovasc. Ther. 3 (2005) 521-535
6. Cao Y.H., Hong A., Schulten H., and Post M.J. Update on therapeutic neovascularization. Cardiovasc. Res. 65 (2005) 639-648
7. de Muinck E.D., and Simons M. Re-evaluating therapeutic neovascularization. J. Mol. Cell Cardiol. 36 (2004) 25-32
8. Patan S. Vasculogenesis and angiogenesis. Cancer Treat. Res. 117 (2004) 3-32
9. Takahashi T., Kalka C., Masuda H., Chen D., Silver M., Kearney M., Magner M., Isner J.M., and Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat. Med. 5 (1999) 434-438
10. Li B., Sharpe E.E., Maupin A.B., Teleron A.A., Pyle A.L., Carmeliet P., and Young P.P. VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J. 20 (2006) E664-E676
11. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6 (2000) 389-395
12. Dvorak H.F. Angiogenesis: update 2005. J. Thromb. Haemost. 3 (2005) 1835-1842
13. Springer M.L. A balancing act: therapeutic approaches for the modulation of angiogenesis. Curr. Opin. Investig. Drugs 7 (2006) 243-250
14. Simons M. Angiogenesis: where do we stand now?. Circulation 111 (2005) 1556-1566
15. Helisch A., and Schaper W. Arteriogenesis: the development and growth of collateral arteries. Microcirculation 10 (2003) 83-97
16. Price R.J., Owens G.K., and Skalak T.C. Immunohistochemical identification of arteriolar development using markers of smooth muscle differentiation. Evidence that capillary arterialization proceeds from terminal arterioles. Circ. Res. 75 (1994) 520-527
17. Jain R.K. Molecular regulation of vessel maturation. Nat. Med. 9 (2003) 685-693
18. Schaper W., and Scholz D. Factors regulating arteriogenesis. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 1143-1151
19. Losordo D.W., and Dimmeler S. Therapeutic angiogenesis and vasculogenesis for ischemic disease. Part I: angiogenic cytokines. Circulation 109 (2004) 2487-2491
20. Chen R.R., and Mooney D.J. Polymeric growth factor delivery strategies for tissue engineering. Pharm. Res. 20 (2003) 1103-1112
21. Takeshita S., Zheng L.P., Brogi E., Kearney M., Pu L.Q., Bunting S., Ferrara N., S.J.F., and Isner J.M. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb mode. J. Clin. Invest. 93 (1994) 662-670
22. Udelson J.E., Dilsizian V., Laham R.J., Chronos N., Vansant J., Blais M., Galt J.R., Pike M., Yoshizawa C., and Simons M. Therapeutic angiogenesis with recombinant fibroblast growth factor-2 improves stress and rest myocardial perfusion abnormalities in patients with severe symptomatic chronic coronary artery disease. Circulation 102 (2000) 1605-1610
23. Schumacher B., Pecher P., von Specht B.U., and Stegmann T. 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
24. Henry T.D., Annex B.H., McKendall G.R., Azrin M.A., Lopez J.J., Giordano F.J., Shah P.K., Willerson J.T., Benza R.L., Berman D.S., Gibson C.M., Bajamonde A., Rundle A.C., Fine J., McCluskey E.R., and VIVA Investigators. The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation 107 (2003) 1359-1365
25. Rajagopalan S., Mohler E.R., Lederman R.J., Mendelsohn F.O., Saucedo J.F., Goldman C.K., Blebea J., Macko J., Kessler P.D., Rasmussen H.S., and Annex B.H. Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation 108 (2003) 1933-1938
26. Simons M., Annex B.H., Laham R.J., Kleiman N., Henry T., Dauerman H., Udelson J.E., Gervino E.V., Pike M., Whitehouse M.J., Moon T., and Chronos N.A. Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial. Circulation 105 (2002) 788-793
27. Ennett A.B., and Mooney D.J. Tissue engineering strategies for in vivo neovascularisation. Expert Opin. Biol. Ther. 2 (2002) 805-818
28. Storrie H., and Mooney D.J. Sustained delivery of plasmid DNA from polymeric scaffolds for tissue engineering. Adv. Drug Deliv. Rev. 58 (2006) 500-514
29. Rafii S., and Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 9 (2003) 702-712
30. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 25 (2004) 581-611
31. Coultas L., Chawengsaksophak K., and Rossant J. Endothelial cells and VEGF in vascular development. Nature 438 (2005) 937-945
32. Ruhrberg C. Growing and shaping the vascular tree: multiple roles for VEGF. BioEssays 25 (2003) 1052-1060
33. Asahara T., Takahashi T., Masuda H., Kalka C., Chen D.H., Iwaguro H., Inai Y., Silver M., and Isner J.M. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 18 (1999) 3964-3972
34. Grunewald M., Avraham I., Dor Y., Bachar-Lustig E., Itin A., Jung S., Chimenti S., Landsman L., Abramovitch R., and Keshet E. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124 (2006) 175-189
35. Alon T., Hemo I., Itin A., Pe'er J., Stone J., and Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat. Med. 1 (1995) 1024-1028
36. Benjamin L.E., and K.E. Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: induction of endothelial cell shedding and regression of hemangioblastoma-like vessels by VEGF withdrawal. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8761-8766
37. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., Eberhardt C., Declercq C., Pawling J., Moons L., Collen D., Risau W., and Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380 (1996) 435-439
38. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., and Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380 (1996) 439-442
39. Miquerol L., Langille B.L., and Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127 (2000) 3941-3946
40. Ferrara N., Gerber H.-P., and LeCouter J. The biology of VEGF and its receptors. Nat. Med. 9 (2003) 669-676
41. Kiefer F.N., Neysari S., Humar R., Li W., Munk V.C., and Battegay E.J. Hypertension and angiogenesis. Curr. Pharm. Des. 9 (2003) 1733-1744
42. Drake C.J., and Little C.D. Exogenous vascular endothelial growth-factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 7657-7661
43. Dor Y., Djonov V., Abramovitch R., Itin A., Fishman G.I., Carmeliet P., Goelman G., and Keshet E. Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J. 21 (2002) 1939-1947
44. Feucht M., Christ B., and Wilting J. VEGF induces cardiovascular malformation and embryonic lethality. Am. J. Pathol. 151 (1996) 1407-1416
45. von Degenfeld G., Banfi A., Springer M.L., Wagner R.A., Jacobi J., Ozawa C.R., Merchant M.J., Cooke J.P., and Blau H.M. Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia. FASEB J. 20 (2006) E2277-E2287
46. Yasuhara T., Shingo T., Muraoka K., Ji Y.W., Kameda M., Takeuchi A., Yano A., Nishio S., Matsui T., Miyoshi Y., Hamada H., and Date I. The differences between high and low-dose administration of VEGF to dopaminergic neurons of in vitro and in vivo Parkinson's disease model. Brain Res. 1038 (2005) 1-10
47. Manoonkitiwongsa P.S., Schultz R.L., McCreery D.B., Whitter E.F., and Lyden P.D. Neuroprotection of ischemic brain by vascular endothelial growth factor is critically dependent on proper dosage and may be compromised by angiogenesis. J. Cereb. Blood Flow Metab. 24 (2004) 693-702
48. Sola F., Gualandris A., Belleri M., Giuliani R., Coltrini D., Bastaki M., Tosatti M.P., Bonardi F., Vecchi A., Fioretti F., Ciomei M., Grandi M., Mantovani A., and Presta M. Endothelial cells overexpressing basic fibroblast growth factor (FGF-2) induce vascular tumors in immunodeficient mice. Angiogenesis 1 (1997) 102-116
49. Lazarous D.F., Shou M., Scheinowitz M., Hodge E., Thirumurti V., Kitsiou A.N., Stiber J.A., Lobo A.D., Hunsberger S., Guetta E., Epstein S.E., and Unger E.F. Comparative effects of basic fibroblast growth factor and vascular endothelial growth factor on coronary collateral development and the arterial response to injury. Circulation 94 (1996) 1074-1082
50. Mitchell C.A., Risau W., and Drexler H.C. Regression of vessels in the tunica vasculosa lentis is initiated by coordinated endothelial apoptosis: a role for vascular endothelial growth factor as a survival factor for endothelium. Dev. Dyn. 213 (1998) 322-333
51. Meeson A.P., Argilla M., Ko K., Witte L., and Lang R.A. VEGF deprivation-induced apoptosis is a component of programmed capillary regression. Development 126 (1999) 1407-1415
52. Gabrilovich D.I., Chen H.L., Girgis K.R., Cunningham H.T., Meny G.M., Nadaf S., Kavanaugh D., and Carbone D.P. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 2 (1996) 1096-1103
53. Laxmanan S., Robertson S.W., Wang E., Lau J.S., Briscoe D.M., and Mukhopadhyay D. Vascular endothelial growth factor impairs the functional ability of dendritic cells through Id pathways. Biochem. Biophys. Res. Commun. 334 (2005) 193-198
54. Hoefer I.E., van Royen N., Buschmann I.R., Piek J.J., and Schaper W. Time course of arteriogenesis following femoral artery occlusion in the rabbit. Cardiovasc. Res. 49 (2001) 609-617
55. Voskuil M., Hoefer I.E., van Royen N., Hua J., de Graaf S., Bode C., Buschmann I.R., and Piek J.J. Abnormal monocyte recruitment and collateral artery formation in monocyte chemoattractant protein-1 deficient mice. Vasc. Med. 9 (2004) 287-292
56. Oshima Y., Oshima S., Nambu H., Kachi S., Takahashi K., Umeda N., Shen J., Dong A., Apte R.S., Duh E., Hackett S.F., Okoye G., Ishibashi K., Handa J., Melia M., Wiegand S., Yancopoulos G., Zack D.J., and Campochiaro P.A. Different effects of angiopoietin-2 in different vascular beds: new vessels are most sensitive. FASEB J. 19 (2005) 963-965
57. Peirce S.M., and Skalak T.C. Microvascular remodeling: a complex continuum spanning angiogenesis to arteriogenesis. Microcirculation 10 (2003) 99-111
58. Tufro A. VEGF spatially directs angiogenesis during metanephric development in vitro. Dev. Biol. 227 (2000) 558-566
59. Grosskreutz CL A.-A.B., Duplaa C., Quinn T.P., Terman B.I., Zetter B., and D'Amore P.A. Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc. Res. 58 (1999) 128-136
60. Makanya A.N., Stauffer D., Ribatti D., Burri P.H., and Djonov V. Microvascular growth, development, and remodeling in the embryonic avian kidney: the interplay between sprouting and intussusceptive angiogenic mechanisms. Microsc. Res. Tech. 66 (2005) 275-288
61. Gerhardt H., and Betsholtz C. How do endothelial cells orientate?. EXS 94 (2005) 3-15
62. Gariano R.F., and Gardner T.W. Retinal angiogenesis in development and disease. Nature 438 (2005) 960-966
63. Indraccolo S., Stievano L., Minuzzo S., Tosello V., Esposito G., Piovan E., Zamarchi R., Chieco-Bianchi L., and Amadori A. Interruption of tumor dormancy by a transient angiogenic burst within the tumor microenvironment. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 4216-4221
64. Carmeliet P., Ng Y.S., Nuyens D., Theilmeier G., Brusselmans K., Cornelissen I., Ehler E., Kakkar V.V., Stalmans I., Mattot V., Perriard J.C., Dewerchin M., Flameng W., Nagy A., Lupu F., Moons L., Collen D., D'Amore P.A., and Shima D.T. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nat. Med. 5 (1999) 491-492
65. Ruhrberg C., Gerhardt H., Golding M., Watson R., Ioannidou S., Fujisawa H., Betsholtz C., and Shima D.T. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16 (2002) 2684-2698
66. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., Jeltsch M., Mitchell C., Alitalo K., Shima D., and Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161 (2003) 1163-1177
67. Lindblom P., Gerhardt H., Liebner S., Abramsson A., Enge M., Hellstrom M., Backstrom G., Fredriksson S., Landegren U., Nystrom H.C., Bergstrom G., Dejana E., Ostman A., Lindahl P., and Betsholtz C. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev. 17 (2003) 1835-1840
68. Bacic M., Edwards N.A., and Merrill M.J. Differential expression of vascular endothelial growth factor (vascular permeability factor) forms in rat tissues. Growth Factors 12 (1995) 11-15
69. Ng Y.S., Rohan R., Sunday M.E., Demello D.E., and D'Amore P.A. Differential expression of VEGF isoforms in mouse during development and in the adult. Dev. Dyn. 220 2 (2001) 112-121
70. Pettersson A., Nagy J.A., Brown L.F., Sundberg C., Morgan E., Jungles S., Carter R., Krieger J.E., Manseau E.J., Harvey V.S., Eckelhoefer I.A., Feng D., Dvorak A.M., Mulligan R.C., and Dvorak H.F. Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab. Invest. 80 (2000) 99-115
71. Leong T.T., Fearon U., and Veale D.J. Angiogenesis in psoriasis and psoriatic arthritis: clues to disease pathogenesis. Curr. Rheumatol. Rep. 7 (2005) 325-329
72. Kvanta A. Ocular angiogenesis: the role of growth factors. Acta Ophthalmol. Scand. 84 (2006) 282-288
73. Ito W.D., Arras M., Scholz D., Winkler B., Htun P., and Schaper W. Angiogenesis but not collateral growth is associated with ischemia after femoral artery occlusion. Am. J. Physiol., Heart Circ. Physiol. 273 (1997) H1255-H1265
74. Buschmann I.R., Hoefer I.E., van Royen N., Katzer E., Braun-Dulleaus R., Heil M., Kostin S., Bode C., and Schaper W. GM-CSF: a strong arteriogenic factor acting by amplification of monocyte function. Atherosclerosis 159 (2001) 343-356
75. Hershey J.C., Baskin E.P., Glass J.D., Hartman H.A., Gilberto D.B., Rogers I.T., and Cook J.J. Revascularization in the rabbit hindlimb: dissociation between capillary sprouting and arteriogenesis. Cardiovasc. Res. 49 (2001) 618-625
76. Voskuil V.R.N.M., Hoefer I.E., Seidler R., Guth B.D., Bode C., Schaper W., Piek J.J., and Buschmann I.R. Modulation of collateral artery growth in a porcine hindlimb ligation model using MCP-1. Am. J. Physiol., Heart Circ. Physiol. 284 (2003) H1422-H1428
77. Martin A., Komada M.R., and Sane D.C. Abnormal angiogenesis in diabetes mellitus. Med. Res. Rev. 23 (2003) 117-145
78. Waltenberger J., Lange J., and Kranz A. Vascular endothelial growth factor-A-induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus - a potential predictor for the individual capacity to develop collaterals. Circulation 102 (2000) 185-190
79. Martinez P., Esbrit P., Rodrigo A., Alvarez-Arroyo M.V., and Martinez M.E. Age-related changes in parathyroid hormone-related protein and vascular endothelial growth factor in human osteoblastic cells. Osteoporos. Int. 13 (2002) 874-881
80. Waltenberger J. Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications. Cardiovasc. Res. 49 (2001) 554-560
81. Eizawa T., Murakami Y., Matsui K., Takahashi M., Muroi K., Amemiya M., Takano R., Kusano E., Shimada K., and Ikeda U. Circulating endothelial progenitor cells are reduced in hemodialysis patients. Curr. Med. Res. Opin. 19 (2003) 627-633
82. Scheubel R.J., Zorn H., Silber R.E., Kuss O., Morawietz H., Holtz J., and S.A. Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J. Am. Coll. Cardiol. 42 (2003) 2073-2080
83. Rakic J.M., Lambert V., Munaut C., Bajou K., Peyrollier K., Alvarez-Gonzalez M.L., Carmeliet P., Foidart J.M., and Noel A. Mice without uPA, tPA, or plasminogen genes are resistant to experimental choroidal neovascularization. Invest. Ophthalmol. Vis. Sci. 44 (2003) 1732-1739
84. Jain R.K., Schlenger K., Hockel M., and Yuan F. Quantitative angiogenesis assays: progress and problems. Nat. Med. 3 (1997) 1203-1208
85. Auerbach R., Lewis R., Shinners B., Kubai L., and Akhtar N. Angiogenesis assays: a critical overview. Clin. Chem. 49 (2003) 32-40
86. Staton C.A., Stribbling S.M., Tazzyman S., Hughes R., Brown N.J., and Lewis C.E. Current methods for assaying angiogenesis in vitro and in vivo. Int. J. Exp. Pathol. 85 (2004) 233-248
87. Hasan J., Shnyder S.D., Bibby M., Double J.A., Bicknel R., and Jayson G.C. Quantitative angiogenesis assays in vivo-a review. Angiogenesis 7 (2004) 1-16
88. Griffith L.G., and Swartz M.A. Capturing complex 3D tissue physiology in vitro. Nat. Rev., Mol. Cell Biol. 7 (2006) 211-224
89. Nakatsu M.N., Sainson R.C.A., Aoto J.N., Taylor K.L., Aitkenhead M., Perez-del-Pulgar S., Carpenter P.M., and Hughes C.C.W. Angiogenic sprouting and capillary lumen formation modeled by human umbilical vein endothelial cells (HUVEC) in fibrin gels: the role of fibroblasts and Angiopoietin-1. Microvasc. Res. 66 (2003) 102-112
90. Nakatsu M.N., Sainson R.C.A., Pérez-del-Pulgar S., Aoto J.N., Aitkenhead M., Taylor K.L., Carpenter P.M., and Hughes C.C.W. VEGF121 and VEGF165 regulate blood vessel diameter through vascular endothelial growth factor receptor 2 in an in vitro angiogenesis model. Lab. Invest. 83 (2003) 1873-1885
91. Nehls V., and Drenckhahn D. A novel, microcarrier-based in vitro assay for rapid and reliable quantification of three-dimensional cell migration and angiogenesis. Microvasc. Res. 50 (1995) 311-322
92. Dietrich F., and Lelkes P.I. Fine-tuning of a three-dimensional microcarrier-based angiogenesis assay for the analysis of endothelial-mesenchymal cell co-cultures in fibrin and collagen gels. Angiogenesis 9 (2006) 111-125
93. Zimrin A.B., Villeponteau B., and Maciag T. Models of in vitro angiogenesis: endothelial cell differentiation on fibrin but not Matrigel is transcriptionally dependent. Biochem. Biophys. Res. Commun. 213 (1995) 630-638
94. Heydarkhan-Hagvall S., Helenius G., Johansson B.R., Li J.Y., Mattsson E., and Risberg B. Co-culture of endothelial cells and smooth muscle cells affects gene expression of angiogenic factors. J. Cell. Biochem. 89 (2003) 1250-1259
95. Korff T., Kimmina S., Martiny-Baron G., and Augustin H.G. Blood vessel maturation in a 3-dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. FASEB J. 15 (2001) 447-457
96. Harvey K., Welch Z., Kovala A.T., Garcia J.G., and English D. Comparative analysis of in vitro angiogenic activities of endothelial cells of heterogeneous origin. Microvasc. Res. 63 (2002) 316-326
97. Carmeliet P., Moons L., Dewerchin M., Mackman N., Luther T., Breier G., Ploplis V., Muller M., Nagy A., Plow E., Gerard R., Edgington T., Risau W., and Collen D. Insights in vessel development and vascular disorders using targeted inactivation and transfer of vascular endothelial growth factor, the tissue factor receptor, and the plasminogen system. Ann. N. Y. Acad. Sci. 811 (1997) 191-206
98. Miller J.C., Pien H.H., Sahani D., Sorensen A.G., and Thrall J.H. Imaging angiogenesis: applications and potential for drug development. J. Natl. Cancer Inst. 97 (2005) 172-187
99. McDonald D.M., and Choyke P.L. Imaging of angiogenesis: from microscope to clinic. Nat. Med. 9 (2003) 713-725
100. Milkiewicz M., Brown M.D., Egginton S., and Hudlicka O. Association between shear stress, angiogenesis, and VEGF in skeletal muscles in vivo. Microcirculation 8 (2001) 229-241
101. Yoshimoto M., Kinuya S., Kawashima A., Nishii R., Yokoyama K., and Kawai K. Radioiodinated VEGF to image tumor angiogenesis in a LS180 tumor xenograft model. Nucl. Med. Biol. 33 (2006) 963-969
102. Amyot F., Camphausen K., Siavosh A., Sackett D., and Gandjbakhche A. Quantitative method to study the network formation of endothelial cells in response to tumor angiogenic factors. Syst. Biol. (Stevenage) 152 (2005) 61-66
103. Richardson T.P., Peters M.C., Ennett A.B., and Mooney D.J. Polymeric system for dual growth factor delivery. Nat. Biotechnol. 19 (2001) 1029-1034
104. Sun Q., Chen R.R., Shen Y., Mooney D.J., Rajagopalan S., and Grossman P.M. Sustained vascular endothelial growth factor delivery enhances angiogenesis and perfusion in ischemic hind limb. Pharm. Res. 22 (2005) 1110-1116
105. Springer M.L., Ip T.K., and Blau H.M. Angiogenesis monitored by perfusion with a space-filling microbead suspension. Mol. Ther. 1 (2000) 82-87
106. Lauffenburger D.A., Chu L.L., French A., Oehrtman G., Reddy C., Wells A., Niyogi S., and Wiley H.S. Engineering dynamics of growth factors and other therapeutic ligands. Biotechnol. Bioeng. 52 (1996) 61-80
107. Mahoney M.J., and Saltzman W.M. Controlled release of proteins to tissue transplants for the treatment of neurodegenerative disorders. J. Pharm. Sci. 85 (1996) 1276-1281
108. Mac Gabhann F., Ji J.W., and Popel A.S. Computational model of vascular endothelial growth factor spatial distribution in muscle and pro-angiogenic cell therapy. PLoS Comput. Biol. 2 9 (2006) 1107-1120
109. Radisic M., Deen W., Langer R., and Vunjak-Novakovic G. Mathematical model of oxygen distribution in engineered cardiac tissue with parallel channel array perfused with culture medium containing oxygen carriers. Am. J. Physiol., Heart Circ. Physiol. 288 (2005) H1278-H1289
110. Filion R.J., and Popel A.S. Intracoronary administration of FGF-2: a computational model of myocardial deposition and retention. Am. J. Physiol., Heart Circ. Physiol. 288 (2005) H263-H279
111. Mac Gabhann Y.M.F., and Popel A.S. Monte Carlo simulations of VEGF binding to cell surface receptors in vitro. BBA-Mol. Cell Res. 1746 (2005) 95-107
112. Sun S.Y., Wheeler M.F., Obeyesekere M., and Patrick C.W. A deterministic model of growth factor-induced angiogenesis. Bull. Math. Biol. 67 (2005) 313-337
113. Mac Gabhann F., Ji J.W., and Popel A.S. VEGF gradients, receptor activation, and sprout guidance in resting and exercising skeletal muscle. J. Appl. Physiol. 102 (2007) 722-734
114. Kelm J.M., Diaz Sanchez-Bustamante C., Ehler E., Hoerstrup S.P., Djonov V., Ittner L., and Fussenegger M. VEGF profiling and angiogenesis in human microtissues. J. Biotechnol. 118 (2005) 213-229
115. Ramakrishnan R., Cheung W.K., Wacholtz M.C., Minton N., and Jusko W.J. Pharmacokinetic and pharmacodynamic modeling of recombinant human erythropoietin after single and multiple doses in healthy volunteers. J. Clin. Pharmacol. 44 (2004) 991-1002
116. Woo S., Krzyzanski W., and Jusko W.J. Pharmacokinetic and pharmacodynamic modeling of recombinant human erythropoietin after intravenous and subcutaneous administration in rats. J. Pharmacol. Exp. Ther. 319 (2006) 1297-1306
117. Freedman S.B., and Isner J.M. Therapeutic angiogenesis for coronary artery disease. Ann. Intern. Med. 136 (2002) 54-71
118. Simons M., and Ware J.A. Therapeutic angiogenesis in cardiovascular disease. Nat. Rev., Drug Discov. 2 (2003) 863-871
119. Langer R. Delivery systems for angiogenesis stimulators and inhibitors. EXS 61 (1992) 327-330
120. Patel Z.S., and Mikos A.G. Angiogenesis with biomaterial-based drug- and cell-delivery systems. J. Biomater. Sci., Polym. Ed. 15 (2004) 701-726
121. Fischbach C., and Mooney D.J. Polymeric systems for bioinspired delivery of angiogenic molecules. Adv. Polym. Sci 203 (2006) 191-221
122. Brey E.M., Uriel S., Greisler H.P., and McIntire L.V. Therapeutic neovascularization: contributions from bioengineering. Tissue Eng. 11 (2005) 567-584
123. Zisch A.H., Lutolf M.P., and Hubbell J.A. Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc. Pathol. 12 (2003) 295-310
124. King T.W., and Patrick C.W.J. 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., A 51 (2000) 383-390
125. Murphy W.L., Peters M.C., Kohn D.H., and Mooney D.J. Sustained release of vascular endothelial growth factor from mineralized poly(lactide-co-glycolide) scaffolds for tissue engineering. Biomaterials 21 (2000) 2521-2527
126. Cleland J.L., Duenas E.T., Park A., Daugherty A., Kahn J., Kowalski J., and Cuthbertson A. Development of poly-(d,l-lactide-coglycolide) microsphere formulations containing recombinant human vascular endothelial growth factor to promote local angiogenesis. J. Control. Release 72 (2001) 13-24
127. Wong C., Inman E., Spaethe R., and Helgerson S. Fibrin-based biomaterials to deliver human growth factors. Thromb. Haemost. 89 (2003) 573-582
128. Steffens G.C., Yao C., Prevel P., Markowicz M., Schenck P., Noah E.M., and Pallua N. Modulation of angiogenic potential of collagen matrices by covalent incorporation of heparin and loading with vascular endothelial growth factor. Tissue Eng. 10 (2004) 1502-1509
129. Augst A.D., Kong H.J., and Mooney D.J. Alginate hydrogels as biomaterials. Macromol. Biosci. 6 (2006) 623-633
130. Silva E.A., and Mooney D.J. Spatiotemporal control of VEGF delivery from injectable hydrogels enhances angiogenesis. J. Thromb. Haemost. 5 (2007) 590-598
131. Lee K.Y., Peters M.C., Anderson K.W., and Mooney D.J. Controlled growth factor release from synthetic extracellular matrices. Nature 408 (2000) 998-1000
132. Ishihara M., Obara K., Nakamura S., Fujita M., Masuoka K., Kanatani Y., Takase B., Hattori H., Morimoto Y., Ishihara M., Maehara T., and Kikuchi M. Chitosan hydrogel as a drug delivery carrier to control angiogenesis. J. Artif. Organs 9 (2006) 8-16
133. Young S., Wong M., Tabata Y., and Mikos A.G. Gelatin as a delivery vehicle for the controlled release of bioactive molecules. J. Control. Release 109 (2005) 256-274
134. Lee K.Y., and Mooney D.J. Hydrogels for tissue engineering. Chem. Rev. 101 (2001) 1869-1879
135. Hoffman A.S. Hydrogels for biomedical applications. Adv. Drug Deliv. Rev. 54 (2002) 3-12
136. Mooney D.J., Baldwin D.F., Suh N.P., Vacanti J.P., and Langer R. Novel approach to fabricate porous sponges of poly(d,l-lactic-co-glycolic acid) without the use of organic solvents. Biomaterials 17 (1996) 1417-1422
137. Ratner B.D. Reducing capsular thickness and enhancing angiogenesis around implant drug release systems. J. Control. Release 78 (2002) 211-218
138. Dziubla T.D., and Lowman A.M. Vascularization of PEG-grafted macroporous hydrogel sponges: a three-dimensional in vitro angiogenesis model using human microvascular endothelial cells. J. Biomed. Mater. Res., A 68 (2004) 603-614
139. Bezuidenhout D., Davies N., and Zilla P. Effect of well defined dodecahedral porosity on inflammation and angiogenesis. ASAIO J. 48 (2002) 465-471
140. Ennett A.B., Kaigler D., and Mooney D.J. Temporally regulated delivery of VEGF in vitro and in vivo. J. Biomed. Mater. Res., A 79 (2006) 176-184
141. Kong H.J., Kaigler D., Kim K., and Mooney D.J. Controlling rigidity and degradation of alginate hydrogels via molecular weight distribution. Biomacromolecules 5 (2004) 1720-1727
142. Boontheekul T., Kong H.J., and Mooney D.J. Controlling alginate gel degradation utilizing partial oxidation and bimodal molecular weight distribution. Biomaterials 26 (2005) 2455-2465
143. Lee K.Y., Bouhadir K.H., and Mooney D.J. Controlled degradation of hydrogels using multi-functional cross-linking molecules. Biomaterials 25 (2004) 2461-2466
144. Peters M.C., Isenberg B.C., Rowley J.A., and Mooney D.J. Release from alginate enhances the biological activity of vascular endothelial growth factor. J. Biomater. Sci., Polym. Ed. 9 (1998) 1267-1278
145. Zisch A.H., Lutolf M.P., Ehrbar M., Raeber G.P., Rizzi S.C., Davies N., Schmokel H., Bezuidenhout D., Djonov V., Zilla P., and Hubbell J.A. Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth. FASEB J. 17 (2003) 2260-2262
146. Seliktar D., Zisch A.H., Lutolf M.P., Wrana J.L., and Hubbell J.A. MMP-2 sensitive, VEGF-bearing bioactive hydrogels for promotion of vascular healing. J. Biomed. Mater. Res., A 68 (2004) 704-716
147. Sohier J., Vlugt T.J., Cabrol N., Van Blitterswijk C., de Groot K., and Bezemer J.M. Dual release of proteins from porous polymeric scaffolds. J. Control. Release 111 (2006) 95-106
148. Peirce S.M., Price R.J., and Skalak T.C. Spatial and temporal control of angiogenesis and arterialization using focal applications of VEGF164 and Ang-1. Am. J. Physiol., Heart Circ. Physiol. 286 (2004) H918-H925
149. Cao R., Bråkenhielm E., Pawliuk R., Wariaro D., Post M.J., Wahlberg E., Leboulch P., and Cao Y.H. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat. Med. 9 (2003) 604-613
150. Chen R.R., Silva E.A., Yuen W.W., and Mooney D.J. Spatio-temporal VEGF and PDGF delivery patterns blood vessel formation and maturation. Pharm. Res. 24 (2007) 258-264
151. Rowley J.A., Madlambayan G., and Mooney D.J. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials. 20 (1999) 45-53
152. Massia S.P., and Hubbell J.A. Human endothelial cell interactions with surface-coupled adhesion peptides on a nonadhesive glass substrate and two polymeric biomaterials. J. Biomed. Mater. Res., A 25 (1991) 223-242
153. Maheshwari G., Brown G., Lauffenburger D.A., Wells A., and Griffith L.G. Cell adhesion and motility depend on nanoscale RGD clustering. J. Cell Sci. 113 (2000) 1677-1686
154. Kong H.J., Boontheekul T., and Mooney D.J. Quantifying the relation between adhesion ligand-receptor bond formation and cell phenotype. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 18534-18539
155. Tsang V.L., and Bhatia S.N. Three-dimensional tissue fabrication. Adv. Drug Deliv. Rev. 56 (2004) 1635-1647
156. LaVan D.A., McGuire T., and Langer R. Small-scale systems for in vivo drug delivery. Nat. Biotechnol. 21 (2003) 1184-1191
157. Staples M., Daniel K., Cima M.J., and Langer R. Application of micro- and nano-electromechanical devices to drug delivery. Pharm. Res. 23 (2006) 847-863
158. Santini J.J.T., Richards A.C., Scheidt R., Cima M.J., and Langer R. Microchips as controlled drug-delivery devices. Angew. Chem., Int. Ed. Engl. 39 (2000) 2396-2407
159. Farokhzad O.C., and Langer R. Nanomedicine: developing smarter therapeutic and diagnostic modalities. Adv. Drug Deliv. Rev. 58 (2006) 1456-1459