Injectable system for spatio-temporally controlled delivery of hypoxia-induced angiogenic signalling

Journal of Controlled Release

Volumn 161, Issue 3, 2012, Pages 852-860

  Hadjipanayi, E ^a   Cheema, U ^b   Hopfner, U ^a   Bauer, A ^a   MacHens, H G ^a   Schilling, A F ^a,c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Center for Applied New Technologies in Engineering for Regenerative Medicine (CANTER)   (Germany)

Author keywords

Angiogenic factor; Hypoxia; Injectable delivery; Spatio temporal control

Indexed keywords

ANGIOGENESIS; ANGIOGENIC FACTOR; CELL MATRIX; CELL-FREE; COLLAGEN CONSTRUCTS; CONCENTRATION-DEPENDENT; CONTROLLED DELIVERY; DOWN-REGULATION; HYPOXIA; IN-VITRO; IN-VIVO; INJECTABLE DELIVERY; INJECTABLE SYSTEMS; LOW TEMPERATURES; MINIMALLY INVASIVE; NANO-POROUS; NON-VIABLE; PRE-CONDITIONING; SPATIO-TEMPORAL; THERMO-RESPONSIVE; TYPE I COLLAGEN;

CELL CULTURE; SOL-GELS; TISSUE;

COLLAGEN;

ANGIOGENIC FACTOR; COLLAGEN; FIBROBLAST GROWTH FACTOR; INTERLEUKIN 8; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CELL FREE SYSTEM; HYPOXIA; INTRACELLULAR SPACE; ISCHEMIA; PRIORITY JOURNAL; TISSUE ENGINEERING;

ANOXIA; COLLAGEN TYPE I; DRUG DELIVERY SYSTEMS; FIBROBLAST GROWTH FACTORS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGELS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INJECTIONS; INTERLEUKIN-8; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84864612103     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.04.048     Document Type: Article

References (50)

1. S. Loges, C. Roncal, and P. Carmeliet Development of targeted angiogenic medicine J. Thromb. Haemost. 7 2009 21 33
2. E.A. Phelps, and A.J. Garcia Update on therapeutic vascularization strategies Regen. Med. 4 2009 65 80
3. L. Cao, and D.J. Mooney Spatiotemporal control over growth factor signaling for therapeutic neovascularization Adv. Drug Deliv. Rev. 59 2007 1340 1350 (Pubitemid 350090012)
4. P. Carmeliet Mechanisms of angiogenesis and arteriogenesis Nat. Med. 6 2000 389 395 (Pubitemid 30208155)
5. G.L. Semenza Regulation of tissue perfusion in mammals by hypoxia-inducible factor 1 Exp. Physiol. 92 2007 988 991 (Pubitemid 47568844)
6. T.H. Patel, H. Kimura, C.R. Weiss, G.L. Semenza, and L.V. Hofmann Constitutively active HIF-1alpha improves perfusion and arterial remodeling in an endovascular model of limb ischemia Cardiovasc. Res. 68 2005 144 154 (Pubitemid 41253565)
7. S. Rey, K. Lee, C.J. Wang, K. Gupta, S. Chen, A. McMillan, N. Bhise, A. Levchenko, and G.L. Semenza Synergistic effect of HIF-1alpha gene therapy and HIF-1-activated bone marrow-derived angiogenic cells in a mouse model of limb ischemia Proc. Natl. Acad. Sci. U. S. A. 106 2009 20399 20404
8. R. Weng, Q. Li, H. Li, M. Yang, and L. Sheng Mimic hypoxia improves angiogenesis in ischaemic random flaps J. Plast. Reconstr. Aesthet. Surg. 63 2010 2152 2159
9. M. Raghunath, Y.S. Wong, M. Farooq, and R. Ge Pharmacologically induced angiogenesis in transgenic zebrafish Biochem. Biophys. Res. Commun. 378 2009 766 771
10. K. Pajusola, J. Kunnapuu, S. Vuorikoski, J. Soronen, H. Andre, T. Pereira, P. Korpisalo, S. Yla-Herttuala, L. Poellinger, and K. Alitalo Stabilized HIF-1alpha is superior to VEGF for angiogenesis in skeletal muscle via adeno-associated virus gene transfer FASEB J. 19 2005 1365 1367 (Pubitemid 41113751)
11. H.J. Knowles, Y.M. Tian, D.R. Mole, and A.L. Harris Novel mechanism of action for hydralazine: induction of hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and angiogenesis by inhibition of prolyl hydroxylases Circ. Res. 95 2004 162 169 (Pubitemid 38988682)
12. A. Namiki, E. Brogi, M. Kearney, E.A. Kim, T.G. Wu, T. Couffinhal, L. Varticovski, and J.M. Isner Hypoxia induces vascular endothelial growth factor in cultured human endothelial cells J. Biol. Chem. 270 1995 31189 31195 (Pubitemid 26012206)
13. U. Cheema, R.A. Brown, B. Alp, and A.J. MacRobert Spatially defined oxygen gradients and vascular endothelial growth factor expression in an engineered 3D cell model Cell. Mol. Life Sci. 65 2008 177 186
14. S.S. Di, Z. Yang, B.M. Wyler von, J. Voelzmann, N. Diehm, I. Baumgartner, and C. Kalka Novel cell-free strategy for therapeutic angiogenesis: in vitro generated conditioned medium can replace progenitor cell transplantation PLoS One 4 2009 e5643
15. M. Kubo, T.S. Li, T. Kamota, M. Ohshima, S.L. Qin, and K. Hamano Increased expression of CXCR4 and integrin alphaM in hypoxia-preconditioned cells contributes to improved cell retention and angiogenic potency J. Cell. Physiol. 220 2009 508 514
16. S.H. Bhang, S.W. Cho, W.G. La, T.J. Lee, H.S. Yang, A.Y. Sun, S.H. Baek, J.W. Rhie, and B.S. Kim Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells Biomaterials 32 2011 2734 2747
17. A.P. Levy A cellular paradigm for the failure to increase vascular endothelial growth factor in chronically hypoxic states Coron. Artery Dis. 10 1999 427 430 (Pubitemid 29419560)
18. A. Yamamoto, H. Takahashi, Y. Kojima, Y. Tsuda, Y. Morio, M. Muramatsu, and Y. Fukuchi Downregulation of angiopoietin-1 and Tie2 in chronic hypoxic pulmonary hypertension Respiration 75 2008 328 338 (Pubitemid 351450405)
19. P. Pichiule, and J.C. LaManna Angiopoietin-2 and rat brain capillary remodeling during adaptation and deadaptation to prolonged mild hypoxia J. Appl. Physiol. 93 2002 1131 1139 (Pubitemid 34919687)
20. F. Luo, D. Wariaro, G. Lundberg, H. Blegen, and E. Wahlberg Vascular growth factor expression in a rat model of severe limb ischemia J. Surg. Res. 108 2002 258 267 (Pubitemid 36062707)
21. B. Olszewska-Pazdrak, T.W. Hein, P. Olszewska, and D.H. Carney Chronic hypoxia attenuates VEGF signaling and angiogenic responses by downregulation of KDR in human endothelial cells Am. J. Physiol. Cell Physiol. 296 2009 C1162 C1170
22. I. Barkefors, S. Le Jan, L. Jakobsson, E. Hejll, G. Carlson, H. Johansson, J. Jarvius, J.W. Park, N.L. Jeon, and J. Kreuger Endothelial cell migration in stable gradients of vascular endothelial growth factor a and fibroblast growth factor 2 - effects on chemotaxis and chemokinesis J. Biol. Chem. 283 2008 13905 13912
23. E.A. Silva, and D.J. Mooney Spatiotemporal control of vascular endothelial growth factor delivery from injectable hydrogels enhances angiogenesis J. Thromb. Haemost. 5 2007 590 598 (Pubitemid 46680694)
24. E.A. Silva, and D.J. Mooney Effects of VEGF temporal and spatial presentation on angiogenesis Biomaterials 31 2010 1235 1241
25. Q. Sun, E.A. Silva, A. Wang, J.C. Fritton, D.J. Mooney, M.B. Schaffler, P.M. Grossman, and S. Rajagopalan Sustained release of multiple growth factors from injectable polymeric system as a novel therapeutic approach towards angiogenesis Pharm. Res. 27 2010 264 271
26. A.K. Ekaputra, G.D. Prestwich, S.M. Cool, and D.W. Hutmacher The three-dimensional vascularization of growth factor-releasing hybrid scaffold of poly (epsilon-caprolactone)/collagen fibers and hyaluronic acid hydrogel Biomaterials 32 2011 8108 8117
27. E. Hadjipanayi, R.A. Brown, V. Mudera, D. Deng, W. Liu, and U. Cheema Controlling physiological angiogenesis by hypoxia-induced signaling J. Control. Release 146 2010 309 317
28. E. Hadjipanayi, U. Cheema, V. Mudera, D. Deng, W. Liu, and R.A. Brown First implantable device for hypoxia-mediated angiogenic induction J. Control. Release 153 2011 217 224
29. K. Park Engineered cell/matrix platform for hypoxia-induced angiogenesis J. Control. Release 153 2011 197
30. K. Ozduman, A. Ozkan, O. Yildirim, M.N. Pamir, M. Gunel, and T. Kilic Temporal expression of angiogenesis-related genes in developing neonatal rodent retina: a novel in vivo model to study cerebral vascular development Neurosurgery 66 2010 538 543
31. P.S. Ray, T. Estrada-Hernandez, H. Sasaki, L. Zhu, and N. Maulik Early effects of hypoxia/reoxygenation on VEGF, ang-1, ang-2 and their receptors in the rat myocardium: implications for myocardial angiogenesis Mol. Cell. Biochem. 213 2000 145 153
32. D.E. Komatsu, and M. Hadjiargyrou Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair Bone 34 2004 680 688 (Pubitemid 38393804)
33. G. Forgacs, S.A. Newman, B. Hinner, C.W. Maier, and E. Sackmann Assembly of collagen matrices as a phase transition revealed by structural and rheologic studies Biophys. J. 84 2003 1272 1280 (Pubitemid 36138758)
34. R.A. Brown, M. Wiseman, C.B. Chuo, U. Cheema, and S.N. Nazhat Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano- and microstructures by plastic compression Adv. Funct. Mater. 15 2005 1762 1770 (Pubitemid 41609635)
35. U. Cheema, Z. Rong, O. Kirresh, A.J. MacRobert, P. Vadgama, and R.A. Brown Oxygen diffusion through collagen scaffolds at defined densities: implications for cell survival in tissue models J. Tissue Eng. Regen. Med. 6 1 2012 77 84 10.1002/term.402 Epub 2011 Feb 10
36. Z.M. Rong, U. Cheema, and P. Vadgama Needle enzyme electrode based glucose diffusive transport measurement in a collagen gel and validation of a simulation model Analyst 131 2006 816 821 (Pubitemid 43962645)
37. A.E. Canfield, F.E. Wren, S.L. Schor, M.E. Grant, and A.M. Schor Aortic endothelial cell heterogeneity in vitro. Lack of association between morphological phenotype and collagen biosynthesis J. Cell Sci. 102 Pt. 4 1992 807 814
38. S. Perez-Amodio, W.M. Tra, H.A. Rakhorst, S.E. Hovius, and J.W. van Neck Hypoxia preconditioning of tissue-engineered mucosa enhances its angiogenic capacity in vitro Tissue Eng. Part A 17 2011 1583 1593
39. T. Potta, C. Chun, and S.C. Song Injectable, dual cross-linkable polyphosphazene blend hydrogels Biomaterials 31 2010 8107 8120
40. J. Davda, and V. Labhasetwar An update on angiogenesis therapy Crit. Rev. Eukaryot. Gene Expr. 11 2001 1 21 (Pubitemid 32994857)
41. T. Heikkila, J. Salonen, J. Tuura, N. Kumar, T. Salmi, D.Y. Murzin, M.S. Hamdy, G. Mul, L. Laitinen, A.M. Kaukonen, J. Hirvonen, and V.P. Lehto Evaluation of mesoporous TCPSi, MCM-41, SBA-15, and TUD-1 materials as API carriers for oral drug delivery Drug Deliv. 14 2007 337 347 (Pubitemid 47265819)
42. J.M. Kanczler, J. Barry, P. Ginty, S.M. Howdle, K.M. Shakesheff, and R.O. Oreffo Supercritical carbon dioxide generated vascular endothelial growth factor encapsulated poly(DL-lactic acid) scaffolds induce angiogenesis in vitro Biochem. Biophys. Res. Commun. 352 2007 135 141 (Pubitemid 44821105)
43. J. Rui, M. Dadsetan, M.B. Runge, R.J. Spinner, M.J. Yaszemski, A.J. Windebank, and H. Wang Controlled release of vascular endothelial growth factor using poly-lactic-co-glycolic acid microspheres: in vitro characterization and application in polycaprolactone fumarate nerve conduits Acta Biomater. 8 2012 511 518
44. J.L. Cleland, E.T. Duenas, A. Park, A. Daugherty, J. Kahn, J. Kowalski, and A. Cuthbertson 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 (Pubitemid 32522340)
45. S.A. Newman, G. Forgacs, B. Hinner, C.W. Maier, and E. Sackmann Phase transformations in a model mesenchymal tissue Phys. Biol. 1 2004 100 109 (Pubitemid 44362306)
46. M.K. Nguyen, and D.S. Lee Injectable biodegradable hydrogels Macromol. Biosci. 10 2010 563 579
47. L. Klouda, and A.G. Mikos Thermoresponsive hydrogels in biomedical applications Eur. J. Pharm. Biopharm. 68 2008 34 45 (Pubitemid 350181413)
48. C. Borselli, H. Storrie, F. esch-Lee, D. Shvartsman, C. Cezar, J.W. Lichtman, H.H. Vandenburgh, and D.J. Mooney Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors Proc. Natl. Acad. Sci. U. S. A. 107 2010 3287 3292
49. I. Ishii, H. Mizuta, A. Sei, J. Hirose, S. Kudo, and Y. Hiraki Healing of full-thickness defects of the articular cartilage in rabbits using fibroblast growth factor-2 and a fibrin sealant J. Bone Joint Surg. Br. 89 2007 693 700 (Pubitemid 46958782)
50. J.R. Hurley, S. Balaji, and D.A. Narmoneva Complex temporal regulation of capillary morphogenesis by fibroblasts Am. J. Physiol. Cell Physiol. 299 2010 C444 C453