Coacervate Delivery of Growth Factors Combined with a Degradable Hydrogel Preserves Heart Function after Myocardial Infarction

ACS Biomaterials Science and Engineering

Volumn 1, Issue 9, 2015, Pages 753-759

  Johnson, Noah Ray ^a,b   Kruger, Maritza ^c   Goetsch, Kyle Peter ^c   Zilla, Peter ^c   Bezuidenhout, Deon ^c   Wang, Yadong ^a,b   Davies, Neil Hamer ^c  

^a University of Pittsburgh   (United States)

^b MCGOWAN INSTITUTE FOR REGENERATIVE MEDICINE   (United States)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

coacervate; controlled release; hydrogel; interleukin 10; myocardial infarction; sonic hedgehog

Indexed keywords

GROWTH FACTOR; INTERLEUKIN 10; MACROGOL; SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COACERVATION; CONTROLLED STUDY; CORONARY ARTERY LIGATION; FLUORESCENCE IMAGING; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE; HYDROGEL; MALE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; RAT; REGENERATIVE MEDICINE; SUSTAINED DRUG RELEASE; VASCULARIZATION;

EID: 84969247891     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/acsbiomaterials.5b00077     Document Type: Article

References (44)

1. Murray, C. J.; Lopez, A. D. Measuring the global burden of disease N. Engl. J. Med. 2013, 369 (5) 448-57 10.1056/NEJMra1201534
2. Go, A. S.; Mozaffarian, D.; Roger, V. L.; Benjamin, E. J.; Berry, J. D.; Blaha, M. J.; Dai, S.; Ford, E. S.; Fox, C. S.; Franco, S.; Fullerton, H. J.; Gillespie, C.; Hailpern, S. M.; Heit, J. A.; Howard, V. J.; Huffman, M. D.; Judd, S. E.; Kissela, B. M.; Kittner, S. J.; Lackland, D. T.; Lichtman, J. H.; Lisabeth, L. D.; Mackey, R. H.; Magid, D. J.; Marcus, G. M.; Marelli, A.; Matchar, D. B.; McGuire, D. K.; Mohler, E. R., 3rd; Moy, C. S.; Mussolino, M. E.; Neumar, R. W.; Nichol, G.; Pandey, D. K.; Paynter, N. P.; Reeves, M. J.; Sorlie, P. D.; Stein, J.; Towfighi, A.; Turan, T. N.; Virani, S. S.; Wong, N. D.; Woo, D.; Turner, M. B. American Heart Association Statistics, C.; Stroke Statistics, S., Heart disease and stroke statistics - 2014 update: a report from the American Heart Association Circulation 2014, 129 (3) e28-e292 10.1161/01.cir.0000441139.02102.80
3. Yusen, R. D.; Edwards, L. B.; Kucheryavaya, A. Y.; Benden, C.; Dipchand, A. I.; Dobbels, F.; Goldfarb, S. B.; Levvey, B. J.; Lund, L. H.; Meiser, B.; Stehlik, J. International Society for, H.; Lung, T., The registry of the International Society for Heart and Lung Transplantation: thirty-first adult lung and heart-lung transplant report - 2014; focus theme: retransplantation J. Heart Lung Transplant 2014, 33 (10) 1009-24 10.1016/j.healun.2014.08.004
4. Radisic, M.; Christman, K. L. Materials science and tissue engineering: repairing the heart Mayo Clin. Proc. 2013, 88 (8) 884-98 10.1016/j.mayocp.2013.05.003
5. Nelson, D. M.; Ma, Z.; Fujimoto, K. L.; Hashizume, R.; Wagner, W. R. Intra-myocardial biomaterial injection therapy in the treatment of heart failure: Materials, outcomes and challenges Acta Biomater. 2011, 7 (1) 1-15 10.1016/j.actbio.2010.06.039
6. Radhakrishnan, J.; Krishnan, U. M.; Sethuraman, S. Hydrogel based injectable scaffolds for cardiac tissue regeneration Biotechnol. Adv. 2014, 32, 449 10.1016/j.biotechadv.2013.12.010
7. Malliaras, K.; Makkar, R. R.; Smith, R. R.; Cheng, K.; Wu, E.; Bonow, R. O.; Marban, L.; Mendizabal, A.; Cingolani, E.; Johnston, P. V.; Gerstenblith, G.; Schuleri, K. H.; Lardo, A. C.; Marban, E. Intracoronary Cardiosphere-Derived Cells After Myocardial Infarction: Evidence of Therapeutic Regeneration in the Final 1-Year Results of the CADUCEUS Trial (CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction) J. Am. Coll. Cardiol. 2014, 63 (2) 110-22 10.1016/j.jacc.2013.08.724
8. Chugh, A. R.; Beache, G. M.; Loughran, J. H.; Mewton, N.; Elmore, J. B.; Kajstura, J.; Pappas, P.; Tatooles, A.; Stoddard, M. F.; Lima, J. A.; Slaughter, M. S.; Anversa, P.; Bolli, R. Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance Circulation 2012, 126 (11 Suppl 1) S54-64 10.1161/CIRCULATIONAHA.112.092627
9. Hamshere, S.; Choudhury, T.; Jones, D. A.; Locca, D.; Mills, P.; Rothman, M.; Knight, C.; Parmar, M.; Agrawal, S.; Martin, J.; Mathur, A. A randomised double-blind control study of early intracoronary autologous bone marrow cell infusion in acute myocardial infarction (REGENERATE-AMI) BMJ. Open 2014, 4 (2) e004258 10.1136/bmjopen-2013-004258
10. Suncion, V. Y.; Ghersin, E.; Fishman, J.; Zambrano, J. P.; Karantalis, V.; Mandel, N. S.; Nelson, K. H.; Gerstenblith, G.; Difede, D. L.; Breton, E.; Sitammagari, K. K.; Schulman, I. H.; Taldone, S.; Williams, A. R.; Sanina, C.; Johnston, P.; Brinker, J. A.; Altman, P. A.; Mushtaq, M.; Trachtenberg, B.; Mendizabal, A.; Tracy, M.; Da Silva, J.; McNiece, I.; Lardo, A.; George, R. T.; Hare, J. M.; Heldman, A. Does Transendocardial Injection of Mesenchymal Stem Cells Improve Myocardial Function Locally or Globally? An Analysis From the POSEIDON Randomized Trial Circ. Res. 2014, 114, 1292 10.1161/CIRCRESAHA.114.302854
11. 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.; Chronos, N. A. Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial Circulation 2002, 105 (7) 788-93 10.1161/hc0802.104407
12. Losordo, D. W.; Vale, P. R.; Hendel, R. C.; Milliken, C. E.; Fortuin, F. D.; Cummings, N.; Schatz, R. A.; Asahara, T.; Isner, J. M.; Kuntz, R. E. Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia Circulation 2002, 105 (17) 2012-2018 10.1161/01.CIR.0000015982.70785.B7
13. Chachques, J. C.; Trainini, J. C.; Lago, N.; Cortes-Morichetti, M.; Schussler, O.; Carpentier, A. Myocardial Assistance by Grafting a New Bioartificial Upgraded Myocardium (MAGNUM trial): clinical feasibility study Ann. Thorac Surg 2008, 85 (3) 901-8 10.1016/j.athoracsur.2007.10.052
14. Ikaria Holdings Inc. IK-5001 for the Preventionof Remodelingof the Ventricle and Congestive Heart Failure After Acute MyocardialInfarction (PRESERVATION I). In: ClinicalTrials. gov [Internet]. Bethesda(MD): National Library of Medicine (US). 2012. NLM Identifier: NCT01226563.
15. Burdick, J. A.; Mauck, R. L.; Gorman, J. H., 3rd; Gorman, R. C. Acellular biomaterials: an evolving alternative to cell-based therapies Sci. Transl. Med. 2013, 5 (176) 176ps4 10.1126/scitranslmed.3003997
16. Lavine, K. J.; Ornitz, D. M. Fibroblast growth factors and Hedgehogs: at the heart of the epicardial signaling center Trends Genet. 2008, 24 (1) 33-40 10.1016/j.tig.2007.10.007
17. Pan, J. Y.; Zhou, S. H. The hedgehog signaling pathway, a new therapeutic target for treatment of ischemic heart disease Pharmazie 2012, 67 (6) 475-81 10.1691/ph.2012.1744
18. Kusano, K. F.; Pola, R.; Murayama, T.; Curry, C.; Kawamoto, A.; Iwakura, A.; Shintani, S.; Ii, M.; Asai, J.; Tkebuchava, T.; Thorne, T.; Takenaka, H.; Aikawa, R.; Goukassian, D.; von Samson, P.; Hamada, H.; Yoon, Y. S.; Silver, M.; Eaton, E.; Ma, H.; Heyd, L.; Kearney, M.; Munger, W.; Porter, J. A.; Kishore, R.; Losordo, D. W. Sonic hedgehog myocardial gene therapy: tissue repair through transient reconstitution of embryonic signaling Nat. Med. 2005, 11 (11) 1197-204 10.1038/nm1313
19. Palladino, M.; Gatto, I.; Neri, V.; Straino, S.; Silver, M.; Tritarelli, A.; Piccioni, A.; Smith, R. C.; Gaetani, E.; Losordo, D. W.; Crea, F.; Capogrossi, M.; Pola, R. Pleiotropic beneficial effects of sonic hedgehog gene therapy in an experimental model of peripheral limb ischemia Mol. Ther. 2011, 19 (4) 658-66 10.1038/mt.2010.292
20. Ahmed, R. P.; Haider, K. H.; Shujia, J.; Afzal, M. R.; Ashraf, M. Sonic Hedgehog gene delivery to the rodent heart promotes angiogenesis via iNOS/netrin-1/PKC pathway PLoS One 2010, 5 (1) e8576 10.1371/journal.pone.0008576
21. Pola, R.; Ling, L. E.; Silver, M.; Corbley, M. J.; Kearney, M.; Blake Pepinsky, R.; Shapiro, R.; Taylor, F. R.; Baker, D. P.; Asahara, T.; Isner, J. M. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors Nat. Med. 2001, 7 (6) 706-11 10.1038/89083
22. Johnson, N. R.; Wang, Y. Controlled delivery of sonic hedgehog morphogen and its potential for cardiac repair PLoS One 2013, 8 (5) e63075 10.1371/journal.pone.0063075
23. Johnson, N. R.; Wang, Y. Coacervate delivery systems for proteins and small molecule drugs Expert Opin. Drug Delivery 2014, 11 (12) 1829-1832 10.1517/17425247.2014.941355
24. Chu, H.; Johnson, N. R.; Mason, N. S.; Wang, Y. A [polycation:heparin] complex releases growth factors with enhanced bioactivity J. Controlled Release 2011, 150 (2) 157-63 10.1016/j.jconrel.2010.11.025
25. Tirelli, N.; Lutolf, M. P.; Napoli, A.; Hubbell, J. A. Poly(ethylene glycol) block copolymers Rev. Mol. Biotechnol. 2002, 90 (1) 3-15 10.1016/S1389-0352(01)00057-5
26. Dobner, S.; Bezuidenhout, D.; Govender, P.; Zilla, P.; Davies, N. A synthetic non-degradable polyethylene glycol hydrogel retards adverse post-infarct left ventricular remodeling J. Card. Failure 2009, 15 (7) 629-36 10.1016/j.cardfail.2009.03.003
27. Kadner, K.; Dobner, S.; Franz, T.; Bezuidenhout, D.; Sirry, M. S.; Zilla, P.; Davies, N. H. The beneficial effects of deferred delivery on the efficiency of hydrogel therapy post myocardial infarction Biomaterials 2012, 33 (7) 2060-6 10.1016/j.biomaterials.2011.11.031
28. de Waal Malefyt, R.; Abrams, J.; Bennett, B.; Figdor, C. G.; de Vries, J. E. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes J. Exp. Med. 1991, 174 (5) 1209-20 10.1084/jem.174.5.1209
29. Popi, A. F.; Lopes, J. D.; Mariano, M. Interleukin-10 secreted by B-1 cells modulates the phagocytic activity of murine macrophages in vitro Immunology 2004, 113 (3) 348-54 10.1111/j.1365-2567.2004.01969.x
30. Deng, B.; Wehling-Henricks, M.; Villalta, S. A.; Wang, Y.; Tidball, J. G. IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration J. Immunol. 2012, 189 (7) 3669-80 10.4049/jimmunol.1103180
31. Lacraz, S.; Nicod, L. P.; Chicheportiche, R.; Welgus, H. G.; Dayer, J. M. IL-10 inhibits metalloproteinase and stimulates TIMP-1 production in human mononuclear phagocytes J. Clin. Invest. 1995, 96 (5) 2304-10 10.1172/JCI118286
32. Sato, T.; Kameyama, T.; Noto, T.; Nakadate, T.; Ueno, H.; Yamada, K.; Inoue, H., The impact of anti-inflammatory cytokines provoked by CD163 positive macrophages on ventricular functional recovery after myocardial infarction. J. Thromb. Thrombolysis 2014. 37, 139 10.1007/s11239-013-0971-3
33. Krishnamurthy, P.; Rajasingh, J.; Lambers, E.; Qin, G.; Losordo, D. W.; Kishore, R. IL-10 inhibits inflammation and attenuates left ventricular remodeling after myocardial infarction via activation of STAT3 and suppression of HuR Circ. Res. 2009, 104 (2) e9-18 10.1161/CIRCRESAHA.108.188243
34. Salek-Ardakani, S.; Arrand, J. R.; Shaw, D.; Mackett, M. Heparin and heparan sulfate bind interleukin-10 and modulate its activity Blood 2000, 96 (5) 1879-1888
35. Pfeffer, M. A.; Pfeffer, J. M.; Fishbein, M. C.; Fletcher, P. J.; Spadaro, J.; Kloner, R. A.; Braunwald, E. Myocardial infarct size and ventricular function in rats Circ. Res. 1979, 44 (4) 503-12 10.1161/01.RES.44.4.503
36. Chu, H.; Gao, J.; Wang, Y. Design, synthesis, and biocompatibility of an arginine-based polyester Biotechnol. Prog. 2012, 28 (1) 257-64 10.1002/btpr.728
37. Ries, C.; Egea, V.; Karow, M.; Kolb, H.; Jochum, M.; Neth, P. MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines Blood 2007, 109 (9) 4055-63 10.1182/blood-2006-10-051060
38. Menasche, P. Cardiac cell therapy: lessons from clinical trials J. Mol. Cell. Cardiol. 2011, 50 (2) 258-65 10.1016/j.yjmcc.2010.06.010
39. Holmes, J. W.; Borg, T. K.; Covell, J. W. Structure and mechanics of healing myocardial infarcts Annu. Rev. Biomed. Eng. 2005, 7, 223-53 10.1146/annurev.bioeng.7.060804.100453
40. Chu, H.; Chen, C. W.; Huard, J.; Wang, Y. The effect of a heparin-based coacervate of fibroblast growth factor-2 on scarring in the infarcted myocardium Biomaterials 2013, 34 (6) 1747-56 10.1016/j.biomaterials.2012.11.019
41. Swynghedauw, B. Molecular mechanisms of myocardial remodeling Physiol Rev. 1999, 79 (1) 215-262
42. Asai, J.; Takenaka, H.; Kusano, K. F.; Ii, M.; Luedemann, C.; Curry, C.; Eaton, E.; Iwakura, A.; Tsutsumi, Y.; Hamada, H.; Kishimoto, S.; Thorne, T.; Kishore, R.; Losordo, D. W. Topical sonic hedgehog gene therapy accelerates wound healing in diabetes by enhancing endothelial progenitor cell-mediated microvascular remodeling Circulation 2006, 113 (20) 2413-24 10.1161/CIRCULATIONAHA.105.603167
43. Stearns, M. E.; Garcia, F. U.; Fudge, K.; Rhim, J.; Wang, M. Role of interleukin 10 and transforming growth factor beta1 in the angiogenesis and metastasis of human prostate primary tumor lines from orthotopic implants in severe combined immunodeficiency mice Clin. Cancer Res. 1999, 5 (3) 711-720
44. Goetsch, K. P.; Bracher, M.; Bezuidenhout, D.; Zilla, P.; Davies, N. H. Regulation of tissue ingrowth into proteolytically degradable hydrogels Acta Biomater. 2015, 10.1016/j.actbio.2015.06.009