Enzymatically-responsive pro-angiogenic peptide-releasing poly(ethylene glycol) hydrogels promote vascularization in vivo

Journal of Controlled Release

Volumn 217, Issue , 2015, Pages 191-201

  Van Hove, Amy H ^a   Burke, Kathleen ^a   Antonienko, Erin ^a   Brown, Edward ^a,b   Benoit, Danielle S W ^a,c  

^a University of Rochester   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Controlled drug release; Enzyme; Hydrogel; Peptide

Indexed keywords

AMINO ACIDS; BIOACTIVITY; DRUG PRODUCTS; ENZYME INHIBITION; ENZYMES; ETHYLENE GLYCOL; PEPTIDES; POLYETHYLENE GLYCOLS; POLYOLS; TISSUE; TISSUE ENGINEERING;

ANGIOGENESIS; CONTROLLED DRUG RELEASE; MATRIX METALLOPROTEINASES; POLY(ETHYLENE GLYCOL) HYDROGEL; REGENERATIVE MEDICINE; THERAPEUTIC ANGIOGENESIS; THERAPEUTIC EFFICACY; TISSUE LOCALIZATION;

HYDROGELS;

GELATINASE A; MACROGOL; OSTEONECTIN; PEPTIDE; SPARC 113; SPARC 118; UNCLASSIFIED DRUG; (2.2.1)BICYCLOHEPT-2-ENE; ANGIOGENIC PROTEIN; BRIDGED BICYCLO COMPOUNDS; DELAYED RELEASE FORMULATION; DRUG CARRIER; HEPTANE; HYDROGEL; MACROGOL DERIVATIVE; OLIGOPEPTIDE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG DEGRADATION; DRUG DELIVERY SYSTEM; FEMALE; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE MEDICINE; SUSTAINED DRUG RELEASE; TISSUE ENGINEERING; VASCULARIZATION; ADMINISTRATION AND DOSAGE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; DELAYED RELEASE FORMULATION; DRUG EFFECTS; METABOLISM; PHARMACOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL;

ANGIOGENIC PROTEINS; ANIMALS; BRIDGED BICYCLO COMPOUNDS; CELLS, CULTURED; DELAYED-ACTION PREPARATIONS; DRUG CARRIERS; FEMALE; HEPTANES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HYDROGELS; MATRIX METALLOPROTEINASE 2; MICE, INBRED BALB C; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGOPEPTIDES; OSTEONECTIN; POLYETHYLENE GLYCOLS;

EID: 84941912426     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.09.005     Document Type: Article

References (59)

1. I. Zachary, and R.D. Morgan Therapeutic angiogenesis for cardiovascular disease: biological context, challenges, prospects Heart 97 2011 181 189
2. M. Lovett, K. Lee, A. Edwards, and D.L. Kaplan Vascularization strategies for tissue engineering Tissue Eng. Part B Rev. 15 2009 353 370
3. D.W. Losordo, and S. Dimmeler Therapeutic angiogenesis and vasculogenesis for ischemic disease. Part I: angiogenic cytokines, Circulation 109 2004 2487 2491
4. E.A. Silva, and D.J. Mooney Effects of VEGF temporal and spatial presentation on angiogenesis Biomaterials 31 2010 1235 1241
5. F. Finetti, A. Basile, D. Capasso, S. Di Gaetano, R. Di Stasi, M. Pascale, C.M. Turco, M. Ziche, L. Morbidelli, and L.D. D'Andrea Functional and pharmacological characterization of a VEGF mimetic peptide on reparative angiogenesis Biochem. Pharmacol. 84 2012 303 311
6. T.F. Lane, M.L. Iruelaarispe, R.S. Johnson, and E.H. Sage Sparc is a source of copper-binding peptides that stimulate angiogenesis J. Cell Biol. 125 1994 929 943
7. B. Hardy, A. Raiter, C. Weiss, B. Kaplan, A. Tenenbaum, and A. Battler Angiogenesis induced by novel peptides selected from a phage display library by screening human vascular endothelial cells under different physiological conditions Peptides 28 2007 691 701
8. D.J. Craik, D.P. Fairlie, S. Liras, and D. Price The future of peptide-based drugs Chem. Biol. Drug Des. 81 2013 136 147
9. J.M. Harris, and R.B. Chess Effect of pegylation on pharmaceuticals Nat. Rev. Drug Discov. 2 2003 214 221
10. A. Van Hove, and D.S. Benoit Depot-based Delivery Systems for Pro-angiogenic Peptides: A Review, Frontiers in Bioengineering and Biotechnology, 3 2015
11. G. Santulli, M. Ciccarelli, G. Palumbo, A. Campanile, G. Galasso, B. Ziaco, G.G. Altobelli, V. Cimini, F. Piscione, L.D. D'Andrea, C. Pedone, B. Trimarco, and G. Iaccarino In vivo properties of the proangiogenic peptide QK J. Transl. Med. 7 2009 41
12. S. Soro, A. Orecchia, L. Morbidelli, P.M. Lacal, V. Morea, K. Ballmer-Hofer, F. Ruffini, M. Ziche, S. D'Atri, G. Zambruno, A. Tramontano, and C.M. Failla A proangiogenic peptide derived from vascular endothelial growth factor receptor-1 acts through alpha 5 beta 1 integrin Blood 111 2008 3479 3488
13. S.A. Ben-Sasson, T. Licht, L. Tsirulnikov, H. Reuveni, and T. Yarnitzky Induction of pro-angiogenic signaling by a synthetic peptide derived from the second intracellular loop of S1P(3) (EDG3) Blood 102 2003 2099 2107
14. S. Choi, M. Baudys, and S.W. Kim Control of blood glucose by novel GLP-1 delivery using biodegradable triblock copolymer of PLGA-PEG-PLGA in type 2 diabetic rats Pharm. Res. 21 2004 827 831
15. A.H. Van Hove, M.J. Beltejar, and D.S. Benoit Development and in vitro assessment of enzymatically-responsive poly(ethylene glycol) hydrogels for the delivery of therapeutic peptides Biomaterials 35 2014 9719 9730
16. E. Jendraschak, and E.H. Sage Regulation of angiogenesis by SPARC and angiostatin: implications for tumor cell biology Semin. Cancer Biol. 7 1996 139 146
17. M.L. Iruelaarispe, T.F. Lane, D. Redmond, M. Reilly, R.P. Bolender, T.J. Kavanagh, and E.H. Sage Expression of Sparc during development of the chicken chorioallantoic membrane - evidence for regulated proteolysis in-vivo Mol. Biol. Cell 6 1995 327 343
18. L. Pickart The human tri-peptide GHK and tissue remodeling J. Biomater. Sci.-Polym. E. 19 2008 969 988
19. K. Motamed SPARC (osteonectin/BM-40) Int. J. Biochem. Cell B 31 1999 1363 1366
20. N.J. Anthis, and G.M. Clore Sequence-specific determination of protein and peptide concentrations by absorbance at 205 nm Protein Sci. 22 2013 851 858
21. B.D. Fairbanks, M.P. Schwartz, A.E. Halevi, C.R. Nuttelman, C.N. Bowman, and K.S. Anseth A versatile synthetic extracellular matrix mimic via thiol-norbornene photopolymerization Adv. Mater. 21 2009 5005 5010
22. E.A. Phelps, N. Landazuri, P.M. Thule, W.R. Taylor, and A.J. Garcia Bioartificial matrices for therapeutic vascularization Proc. Natl. Acad. Sci. U.S.A. 107 2010 3323 3328
23. A.H. Van Hove, E. Antonienko, K. Burke, E. Brown 3rd, and D.S. Benoit Temporally Tunable, Enzymatically Responsive Delivery of Proangiogenic Peptides from Poly(Ethylene Glycol) Hydrogels 2015 Adv Healthc Mater
24. J. Patterson, and J.A. Hubbell Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2 Biomaterials 31 2010 7836 7845
25. M. Ehrbar, A. Metters, P. Zammaretti, J.A. Hubbell, and A.H. Zisch Endothelial cell proliferation and progenitor maturation by fibrin-bound VEGF variants with differential susceptibilities to local cellular activity J. Control. Release 101 2005 93 109
26. J. Siepmann, R.A. Siegel, and M.J. Rathbone Fundamentals and Applications of Controlled Release Drug Delivery, in 2012 Springer US
27. C.A. Schneider, W.S. Rasband, and K.W. Eliceiri NIH image to ImageJ: 25 years of image analysis Nat. Methods 9 2012 671 675
28. A. Niemisto, V. Dunmire, O. Yli-Harja, W. Zhang, and I. Shmulevich Robust quantification of in vitro angiogenesis through image analysis IEEE Trans. Med. Imaging 24 2005 549 553
29. C. Deng, P.C. Zhang, B. Vulesevic, D. Kuraitis, F.F. Li, A.F. Yang, M. Griffith, M. Ruel, and E.J. Suuronen A collagen-chitosan hydrogel for endothelial differentiation and angiogenesis Tissue Eng. Part A 16 2010 3099 3109
30. Y. Tabata, M. Miyao, M. Ozeki, and Y. Ikada Controlled release of vascular endothelial growth factor by use of collagen hydrogels J. Biomat. Sci.-Polym. E 11 2000 915 930
31. G. Sun, Y.I. Shen, S. Kusuma, K. Fox-Talbot, C.J. Steenbergen, and S. Gerecht Functional neovascularization of biodegradable dextran hydrogels with multiple angiogenic growth factors Biomaterials 32 2011 95 106
32. M.D. Hoffman, A.H. Van Hove, and D.S. Benoit Degradable hydrogels for spatiotemporal control of mesenchymal stem cells localized at decellularized bone allografts Acta Biomater. 10 2014 3431 3441
33. A.V. Belo, L.S. Barcelos, M.A.N.D. Ferreira, M.M. Teixeira, and S.P. Andrade Inhibition of inflammatory angiogenesis by distant subcutaneous tumor in mice Life Sci. 74 2004 2827 2837
34. S.P. Andrade, R.D.P. Machado, A.S. Teixeira, A.V. Belo, A.M. Tarso, and W.T. Beraldo Sponge-induced angiogenesis in mice and the pharmacological reactivity of the neovasculature quantitated by a fluorimetric method Microvasc. Res. 54 1997 253 261
35. L.S. Barcelos, A. Talvani, A.S. Teixeira, G.D. Cassali, S.P. Andrade, and M.M. Teixeira Production and in vivo effects of chemokines CXCL1-3/KC and CCL2/JE in a model of inflammatory angiogenesis in mice Inflamm. Res. 53 2004 576 584
36. W.H. Zhu, A. MacIntyre, and R.F. Nicosia 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
37. M. Shibuya Vascular endothelial growth factor (VEGF) and its receptor (VEGFR) signaling in angiogenesis: a crucial target for anti- and pro-angiogenic therapies Genes Cancer 2 2011 1097 1105
38. J.A. Garciasainz, and J.A. Olivaresreyes Glycyl-histidyl-lysine interacts with the angiotensin-Ii at(1) receptor Peptides 16 1995 1203 1207
39. H. Yang, D. Lu, and M.K. Raizada Angiotensin II-induced phosphorylation of the AT(1) receptor from rat brain neurons Hypertension 30 1997 351 357
40. P.J. Gagne, N. Tihonov, X.L. Li, J. Glaser, J.R. Qiao, M. Silberstein, H. Yee, E. Gagne, and P. Brooks Temporal exposure of cryptic collagen epitopes within ischemic muscle during hindlimb reperfusion Am. J. Pathol. 167 2005 1349 1359
41. S.P. Zustiak, and J.B. Leach Hydrolytically degradable poly(ethylene glycol) hydrogel scaffolds with tunable degradation and mechanical properties Biomacromolecules 11 2010 1348 1357
42. H.P. Erickson Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy, Biol. Proced. Online 11 2009 32 51
43. A.H. Zisch, M.P. Lutolf, M. Ehrbar, G.P. Raeber, S.C. Rizzi, N. Davies, H. Schmokel, D. Bezuidenhout, D.V.P. Zilla, and J.A. Hubbell Cell-demanded release of VEGF from synthetic, biointeractive cell-ingrowth matrices for vascularized tissue growth FASEB J. 17 2003 2260 2262
44. N. Artzi, N. Oliva, C. Puron, S. Shitreet, S. Artzi, A.B. Ramos, A. Groothuis, G. Sahagian, and E.R. Edelman In vivo and in vitro tracking of erosion in biodegradable materials using non-invasive fluorescence imaging Nat. Mater. 10 2011 896-896 (vol 10, pg 704, 2011)
45. B.E. Muhs, G. Plitas, Y. Delgado, I. Ianus, J.P. Shaw, M.A. Adelman, P. Lamparello, P. Shamamian, and P. Gagne Temporal expression and activation of matrix metalloproteinases-2,-9, and membrane type 1 - matrix metalloproteinase following acute hindlimb ischemia J. Surg. Res. 111 2003 8 15
46. J.P.M. Cleutjens, J.C. Kandala, E. Guarda, R.V. Guntaka, and K.T. Weber Regulation of collagen degradation in the rat myocardium after infarction J. Mol. Cell. Cardiol. 27 1995 1281 1292
47. B.E. Turk, L.L. Huang, E.T. Piro, and L.C. Cantley Determination of protease cleavage site motifs using mixture-based oriented peptide libraries Nat. Biotechnol. 19 2001 661 667
48. 2 + stimulates matrix metalloproteinase-2 expression by fibroblast cultures Life Sci. 67 2000 2257 2265
49. 2 + J. Invest. Dermatol. 112 1999 957 964
50. Y.P. Han, T.L. Tuan, H.Y. Wu, M. Hughes, and W.L. Garner TNF-alpha stimulates activation of pro-MMP2 in human skin through NF-kappa B mediated induction of MT1-MMP J. Cell Sci. 114 2001 131 139
51. H. Shih, and C.C. Lin Cross-linking and degradation of step-growth hydrogels formed by thiol-ene photoclick chemistry Biomacromolecules 13 2012 2003 2012
52. Z. Xia, and J.T. Triffitt A review on macrophage responses to biomaterials Biomed. Mater. 1 2006 R1 R9
53. E.B. Brown, R.B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R.K. Jain In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy Nat. Med. 7 2001 864 868
54. D. Seliktar, A.H. Zisch, M.P. Lutolf, J.L. Wrana, and J.A. Hubbell MMP-2 sensitive VEGF-bearing bioactive hydrogels for promotion of vascular healing J. Biomed. Mater. Res. A 68A 2004 704 716
55. J.D. Pollard, S. Quan, T. Kang, and R.J. Koch Effects of copper tripeptide on the growth and expression of growth factors by normal and irradiated fibroblasts Arch. Facial. Plast. S 7 2005 27 31
56. S. Jose, M.L. Hughbanks, B.Y. Binder, G.C. Ingavle, and J.K. Leach Enhanced trophic factor secretion by mesenchymal stem/stromal cells with glycine-histidine-lysine (GHK)-modified alginate hydrogels Acta Biomater. 10 2014 1955 1964
57. W.L. Murphy, M.C. Peters, D.H. Kohn, and D.J. Mooney Sustained release of vascular endothelial growth factor from mineralized poly(lactide-co-glycolide) scaffolds for tissue engineering Biomaterials 21 2000 2521 2527
58. M.P. Lutolf, J.L. Lauer-Fields, H.G. Schmoekel, A.T. Metters, F.E. Weber, G.B. Fields, and J.A. Hubbell Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics Proc. Natl. Acad. Sci. U.S.A. 100 2003 5413 5418
59. M.D. Hoffman, C. Xie, X. Zhang, and D.S. Benoit The effect of mesenchymal stem cells delivered via hydrogel-based tissue engineered periosteum on bone allograft healing Biomaterials 34 2013 8887 8898