Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues

Biomaterials

Volumn 31, Issue 2, 2010, Pages 226-241

  Chiu, Loraine L Y ^a   Radisic, Milica ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Angiogenesis; Cardiac tissue engineering; Collagen; Endothelial cell; Growth factors; Scaffold

Indexed keywords

ALTERNATIVE METHODS; ANGIOGENESIS; ANGIOGENIC GROWTH FACTORS; ANGIOPOIETINS; CARBODIIMIDE HYDROCHLORIDES; CARDIAC TISSUE ENGINEERING; CELL NUMBER; CHORIOALLANTOIC MEMBRANE ASSAYS; COLLAGEN SCAFFOLDS; COVALENT IMMOBILIZATION; CULTURE MEDIUM; ENGINEERED TISSUES; GLUCOSE CONSUMPTION RATE; GROWTH FACTOR; GROWTH FACTORS; IN-VITRO; LOCALIZED EFFECTS; PRODUCTION RATES; TUBE FORMATION; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR STRUCTURES; VASCULARIZATION; VON WILLEBRAND FACTOR;

BIOACTIVITY; BIOLOGICAL MATERIALS; BLOOD VESSEL PROSTHESES; CELL CULTURE; COLLAGEN; ENDOTHELIAL CELLS; GLUCOSE; PEPTIDES; SELF ASSEMBLY; TISSUE ENGINEERING;

SCAFFOLDS;

1 (3 DIMETHYLAMINOPROPYL) 3 ETHYLCARBODIIMIDE; ANGIOPOIETIN 1; BIOMATERIAL; CD3 ANTIGEN; COLLAGEN; EOSIN; GLUCOSE; HEMATOXYLIN; LACTIC ACID; TISSUE SCAFFOLD; VASCULOTROPIN; VON WILLEBRAND FACTOR;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL CULTURE; CELL DEATH; CELL INFILTRATION; CELL PROLIFERATION; CELL VIABILITY; CHORIOALLANTOIS; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; ENDOTHELIUM CELL; GLUCOSE INTAKE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POROSITY; PRIORITY JOURNAL; TISSUE ENGINEERING; VASCULARIZATION;

ANGIOPOIETIN-1; ANIMALS; BIOLOGICAL ASSAY; CELL LINE; CELL PROLIFERATION; CELL SHAPE; CHICKENS; CHORIOALLANTOIC MEMBRANE; COLLAGEN; COLLAGENASES; ENDOTHELIAL CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEMOGLOBINS; HUMANS; HYDROLYSIS; IMMOBILIZED PROTEINS; MICE; MICROSCOPY, ELECTRON, SCANNING; NEOVASCULARIZATION, PHYSIOLOGIC; SOLUBILITY; TISSUE ENGINEERING; TISSUE SCAFFOLDS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70350726213     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2009.09.039     Document Type: Article

References (69)

1. Radisic M., Malda J., Epping E., Geng W., Langer R., and Vunjak-Novakovic G. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng 93 (2006) 332-343
2. Rakusan K., and Korecky B. The effect of growth and aging on functional capillary supply of the rat heart. Growth 46 (1982) 275-281
3. Fidkowski C., Kaazempur-Mofrad M.R., Borenstein J., Vacanti J.P., Langer R., and Wang Y. Endothelialized microvasculature based on a biodegradable elastomer. Tissue Eng 11 (2005) 302-309
4. Lee H., Chung H.J., and Park T.G. Perspectives on: local and sustained delivery of angiogenic growth factors. J Bioact Compat Polym 22 (2007) 89-114
5. Radisic M., Yang L., Boublik J., Cohen R.J., Langer R., Freed L.E., et al. Medium perfusion enables engineering of compact and contractile cardiac tissue. Am J Physiol Heart Circ Physiol 286 (2004) H507-H516
6. Brown M., Iyer R., and Radisic M. Pulsatile perfusion bioreactor for cardiac tissue engineering. Biotechnol Prog 24 (2008) 907-920
7. Tsuda Y., Shimizu T., Yamato M., Kikuchi A., Sasagawa T., Sekiya S., et al. Cellular control of tissue architectures using a three-dimensional tissue fabrication technique. Biomaterials 28 (2007) 4939-4946
8. Radisic M., Park H., Chen F., Salazar-Lazzaro J.E., Wang Y., Dennis R., et al. Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 12 (2006) 2077-2091
9. Morritt A.N., Bortolotto S.K., Dilley R.J., Han X., Kompa A.R., McCombe D., et al. Cardiac tissue engineering in an in vivo vascularized chamber. Circulation 115 (2007) 353-360
10. Jiang F., Zhang G., Hashimoto I., Kumar B.S., Bortolotto S., Morrison W.A., et al. Neovascularization in an arterio-venous loop-containing tissue engineering chamber: role of NADPH oxidase. J Cell Mol Med 12 (2008) 2062-2072
11. 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
12. Tabata Y., Miyao M., Ozeki M., and Ikada Y. Controlled release of vascular endothelial growth factor by use of collagen hydrogels. J Biomater Sci Polym Ed 11 (2000) 915-930
13. Hao X., Silva E.A., Mansson-Broberg A., Grinnemo K.H., Siddiqui A.J., Dellgren G., et al. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc Res 75 (2007) 178-185
14. Steffens G.C., Yao C., Prevel P., Markowicz M., Schenck P., Noah E.M., et al. 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
15. Hosack L.W., Firpo M.A., Scott J.A., Prestwich G.D., and Peattie R.A. Microvascular maturity elicited in tissue treated with cytokine-loaded hyaluronan-based hydrogels. Biomaterials 29 (2008) 2336-2347
16. Riley C.M., Fuegy P.W., Firpo M.A., Shu X.Z., Prestwich G.D., and Peattie R.A. Stimulation of in vivo angiogenesis using dual growth factor-loaded crosslinked glycosaminoglycan hydrogels. Biomaterials 27 (2006) 5935-5943
17. Zhou L., Ma W., Yang Z., Zhang F., Lu L., Ding Z., et al. VEGF165 and angiopoietin-1 decreased myocardium infarct size through phosphatidylinositol-3 kinase and Bcl-2 pathways. Gene Ther 12 (2005) 196-202
18. Ferrara N., Gerber H.P., and LeCouter J. The biology of VEGF and its receptors. Nat Med 9 (2003) 669-676
19. Zacchigna S., Tasciotti E., Kusmic C., Arsic N., Sorace O., Marini C., et al. In vivo imaging shows abnormal function of vascular endothelial growth factor-induced vasculature. Hum Gene Ther 18 (2007) 515-524
20. Morisada T., Kubota Y., Urano T., Suda T., and Oike Y. Angiopoietins and angiopoietin-like proteins in angiogenesis. Endothelium 13 (2006) 71-79
21. Kwak H.J., Lee S.J., Lee Y.H., Ryu C.H., Koh K.N., Choi H.Y., et al. Angiopoietin-1 inhibits irradiation- and mannitol-induced apoptosis in endothelial cells. Circulation 101 (2000) 2317-2324
22. Dallabrida S.M., Ismail N., Oberle J.R., Himes B.E., and Rupnick M.A. Angiopoietin-1 promotes cardiac and skeletal myocyte survival through integrins. Circ Res 96 (2005) e8-e24
23. Wang Z., Cui M., Sun L., Jia Z., Bai Y., Ma K., et al. Angiopoietin-1 protects H9c2 cells from H2O2-induced apoptosis through AKT signaling. Biochem Biophys Res Commun 359 (2007) 685-690
24. Kim S.H., and Kiick K.L. Heparin-mimetic sulfated peptides with modulated affinities for heparin-binding peptides and growth factors. Peptides 28 (2007) 2125-2136
25. Gavard J., Patel V., and Gutkind J.S. Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia. Dev Cell 14 (2008) 25-36
26. Arsic N., Zentilin L., Zacchigna S., Santoro D., Stanta G., Salvi A., et al. Induction of functional neovascularization by combined VEGF and angiopoietin-1 gene transfer using AAV vectors. Mol Ther 7 (2003) 450-459
27. DeBusk L.M., Hallahan D.E., and Lin P.C. Akt is a major angiogenic mediator downstream of the Ang1/Tie2 signaling pathway. Exp Cell Res 298 (2004) 167-177
28. Chen H.K., Hung H.F., Shyu K.G., Wang B.W., Sheu J.R., Liang Y.J., et al. Combined cord blood stem cells and gene therapy enhances angiogenesis and improves cardiac performance in mouse after acute myocardial infarction. Eur J Clin Invest 35 (2005) 677-686
29. Benest A.V., Salmon A.H., Wang W., Glover C.P., Uney J., Harper S.J., et al. VEGF and angiopoietin-1 stimulate different angiogenic phenotypes that combine to enhance functional neovascularization in adult tissue. Microcirculation 13 (2006) 423-437
30. Zhu W.H., MacIntyre A., and Nicosia R.F. Regulation of angiogenesis by vascular endothelial growth factor and angiopoietin-1 in the rat aorta model: distinct temporal patterns of intracellular signaling correlate with induction of angiogenic sprouting. Am J Pathol 161 (2002) 823-830
31. Cheng M., Park H., Engelmayr G.C., Moretti M., and Freed L.E. Effects of regulatory factors on engineered cardiac tissue in vitro. Tissue Eng 13 (2007) 2709-2719
32. George M.L., Eccles S.A., Tutton M.G., Abulafi A.M., and Swift R.I. Correlation of plasma and serum vascular endothelial growth factor levels with platelet count in colorectal cancer: clinical evidence of platelet scavenging?. Clin Cancer Res 6 (2000) 3147-3152
33. Boontheekul T., and Mooney D.J. Protein-based signaling systems in tissue engineering. Curr Opin Biotechnol 14 (2003) 559-565
34. Jain R.K., Au P., Tam J., Duda D.G., and Fukumura D. Engineering vascularized tissue. Nat Biotechnol 23 (2005) 821-823
35. Shen Y.H., Shoichet M.S., and Radisic M. Vascular endothelial growth factor immobilized in collagen scaffold promotes penetration and proliferation of endothelial cells. Acta Biomater 4 (2008) 477-489
36. Ito Y. Covalently immobilized biosignal molecule materials for tissue engineering. Soft Matter 4 (2008) 46-56
37. Chiu L.L., Iyer R.K., King J.P., and Radisic M. Biphasic electrical field stimulation aids in tissue engineering of multicell-type cardiac organoids. Tissue Eng Part A (2008)
38. Chen P.R., Chen M.H., Lin F.H., and Su W.Y. Release characteristics and bioactivity of gelatin-tricalcium phosphate membranes covalently immobilized with nerve growth factors. Biomaterials 26 (2005) 6579-6587
39. Leclerc C., Brose C., Nouze C., Leonard F., Majlessi L., Becker S., et al. Immobilized cytokines as biomaterials for manufacturing immune cell based vaccines. J Biomed Mater Res A 86 (2008) 1033-1040
40. von Walter M., Herren C., Gensior T.J., Steffens G.C., Hermanns-Sachweh B., Jahnen-Dechent W., et al. Biomimetic modification of the TiO(2)/glass composite Ecopore with heparinized collagen and the osteoinductive factor BMP-2. Acta Biomater 4 (2008) 997-1004
41. West D.C., Thompson W.D., Sells P.G., and Burbridge M.F. Angiogenesis assays using chick chorioallantoic membrane. In: Murray J. (Ed). Angiogenesis protocols (2001), Humana Press, New Jersey 107-129
42. Ghosh K., Pan Z., Guan E., Ge S., Liu Y., Nakamura T., et al. Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials 28 (2007) 671-679
43. Park H., Radisic M., Lim J.O., Chang B.H., and Vunjak-Novakovic G. A novel composite scaffold for cardiac tissue engineering. In Vitro Cell Dev Biol Anim 41 (2005) 188-196
44. Callegari A., Bollini S., Iop L., Chiavegato A., Torregrossa G., Pozzobon M., et al. Neovascularization induced by porous collagen scaffold implanted on intact and cryoinjured rat hearts. Biomaterials 28 (2007) 5449-5461
45. Radisic M., Fast V.G., Sharifov O.F., Iyer R.K., Park H., and Vunjak-Novakovic G. Optical mapping of impulse propagation in engineered cardiac tissue. Tissue Eng Part A 15 (2009) 851-860
46. Metheny-Barlow L.J., Tian S., Hayes A.J., and Li L.Y. Direct chemotactic action of angiopoietin-1 on mesenchymal cells in the presence of VEGF. Microvasc Res 68 (2004) 221-230
47. Grabarek Z., and Gergely J. Zero-length crosslinking procedure with the use of active esters. Anal Biochem 185 (1990) 131-135
48. Cross M.J., Dixelius J., Matsumoto T., and Claesson-Welsh L. VEGF-receptor signal transduction. Trends Biochem Sci 28 (2003) 488-494
49. Bogdanovic E., Nguyen V.P., and Dumont D.J. Activation of Tie2 by angiopoietin-1 and angiopoietin-2 results in their release and receptor internalization. J Cell Sci 119 (2006) 3551-3560
50. Wu F.T., Stefanini M.O., Mac Gabhann F., and Popel A.S. A compartment model of VEGF distribution in humans in the presence of soluble VEGF receptor-1 acting as a ligand trap. PLoS One 4 (2009) e5108
51. Cho C.H., Kammerer R.A., Lee H.J., Steinmetz M.O., Ryu Y.S., Lee S.H., et al. COMP-Ang1: a designed angiopoietin-1 variant with nonleaky angiogenic activity. Proc Natl Acad Sci U S A 101 (2004) 5547-5552
52. Garlanda C., Parravicini C., Sironi M., De Rossi M., Wainstok de Calmanovici R., Carozzi F., et al. Progressive growth in immunodeficient mice and host cell recruitment by mouse endothelial cells transformed by polyoma middle-sized T antigen: implications for the pathogenesis of opportunistic vascular tumors. Proc Natl Acad Sci U S A 91 (1994) 7291-7295
53. Feraud O., Cao Y., and Vittet D. Embryonic stem cell-derived embryoid bodies development in collagen gels recapitulates sprouting angiogenesis. Lab Invest 81 (2001) 1669-1681
54. Balconi G., Spagnuolo R., and Dejana E. Development of endothelial cell lines from embryonic stem cells: A tool for studying genetically manipulated endothelial cells in vitro. Arterioscler Thromb Vasc Biol 20 (2000) 1443-1451
55. Zhou Z., Christofidou-Solomidou M., Garlanda C., and DeLisser H.M. Antibody against murine PECAM-1 inhibits tumor angiogenesis in mice. Angiogenesis 3 (1999) 181-188
56. Kroon M.E., Koolwijk P., van der Vecht B., and van Hinsbergh V.W. Urokinase receptor expression on human microvascular endothelial cells is increased by hypoxia: implications for capillary-like tube formation in a fibrin matrix. Blood 96 (2000) 2775-2783
57. Kutryk M.J., and Stewart D.J. Angiogenesis of the heart. Microsc Res Tech 60 (2003) 138-158
58. Kumar P., Benedict R., Urzua F., Fischbach C., Mooney D., and Polverini P. Combination treatment significantly enhances the efficacy of antitumor therapy by preferentially targeting angiogenesis. Lab Invest 85 (2005) 756-767
59. Saito M., Hamasaki M., and Shibuya M. Induction of tube formation by angiopoietin-1 in endothelial cell/fibroblast co-culture is dependent on endogenous VEGF. Cancer Sci 94 (2003) 782-790
60. Jho D., Mehta D., Ahmmed G., Gao X.P., Tiruppathi C., Broman M., et al. Angiopoietin-1 opposes VEGF-induced increase in endothelial permeability by inhibiting TRPC1-dependent Ca2 influx. Circ Res 96 (2005) 1282-1290
61. Oates M., Chen R., Duncan M., and Hunt J.A. The angiogenic potential of three-dimensional open porous synthetic matrix materials. Biomaterials 28 (2007) 3679-3686
62. Cascone I., Napione L., Maniero F., Serini G., and Bussolino F. Stable interaction between alpha5beta1 integrin and Tie2 tyrosine kinase receptor regulates endothelial cell response to Ang-1. J Cell Biol 170 (2005) 993-1004
63. Wilting J., Christ B., Bokeloh M., and Weich H.A. In vivo effects of vascular endothelial growth factor on the chicken chorioallantoic membrane. Cell Tissue Res 274 (1993) 163-172
64. Fujita M., Ishihara M., Simizu M., Obara K., Ishizuka T., Saito Y., et al. Vascularization in vivo caused by the controlled release of fibroblast growth factor-2 from an injectable chitosan/non-anticoagulant heparin hydrogel. Biomaterials 25 (2004) 699-706
65. Lee R.J., Springer M.L., Blanco-Bose W.E., Shaw R., Ursell P.C., and Blau H.M. VEGF gene delivery to myocardium: deleterious effects of unregulated expression. Circulation 102 (2000) 898-901
66. Yamamura N., Sudo R., Ikeda M., and Tanishita K. Effects of the mechanical properties of collagen gel on the in vitro formation of microvessel networks by endothelial cells. Tissue Eng 13 (2007) 1443-1453
67. Peyton S.R., Raub C.B., Keschrumrus V.P., and Putnam A.J. The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells. Biomaterials 27 (2006) 4881-4893
68. Drury J.L., and Mooney D.J. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24 (2003) 4337-4351
69. Pelham Jr. R.J., and Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A 94 (1997) 13661-13665