Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction

Science Translational Medicine

Volumn 5, Issue 173, 2013, Pages

  Seif Naraghi, Sonya B ^a   Singelyn, Jennifer M ^a   Salvatore, Michael A ^b   Osborn, Kent G ^a   Wang, Jean J ^a   Sampat, Unatti ^a   Kwan, Oi Ling ^a   Strachan, G Monet ^a   Wong, Jonathan ^c   Schup Magoffin, Pamela J ^a   Braden, Rebecca L ^a   Bartels, Kendra ^a   DeQuach, Jessica A ^b   Preul, Mark ^d   Kinsey, Adam M ^b   DeMaria, Anthony N ^a   Dib, Nabil ^a   Christman, Karen L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Ventrix Inc   (United States)

^c Biologics Delivery Systems   (United States)

^d BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIAL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCOMPATIBILITY; BLOOD CLOTTING TIME; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENDOCARDIUM; EXTRACELLULAR MATRIX; FEMALE; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE; HEART VENTRICLE VOLUME; HEART VENTRICLE WALL MOTION; HUMAN; HYDROGEL; IMMUNE RESPONSE; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RAT; SAFETY; THROMBOCYTE ACTIVATION; TREATMENT OUTCOME;

ANIMALS; BIOCOMPATIBLE MATERIALS; EXTRACELLULAR MATRIX; HYDROGELS; MYOCARDIAL INFARCTION; SWINE;

EID: 84874701815     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005503     Document Type: Article

References (37)

1. V. L. Roger, A. S. Go, D. M. Lloyd-Jones, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, B.M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D.M.Makuc, G.M.Marcus, A. Marelli, D. B. Matchar, C. S. Moy, D. Mozaffarian, M. E. Mussolino, G. Nichol, N. P. Paynter, E. Z. Soliman, P.D. Sorlie, N. Sotoodehnia, T. N. Turan, S. S. Virani, N.D. Wong, D. Woo, M. B. Turner; American Heart Association Statistics Committee and Stroke Statistics Subcommittee, Heart disease and stroke statistics - 2012 update: A report from the American Heart Association. Circulation 125, e2-e220 (2012).
2. K. L. Christman, R. J. Lee, Biomaterials for the treatment of myocardial infarction. J. Am. Coll. Cardiol. 48, 907-913 (2006).
3. A. A. Rane, K. L. Christman, Biomaterials for the treatment of myocardial infarction: A 5-year update. J. Am. Coll. Cardiol. 58, 2615-2629 (2011).
4. D. M. Nelson, Z. Ma, K. L. Fujimoto, R. Hashizume, W. R. Wagner, Intra-myocardial biomaterial injection therapy in the treatment of heart failure: Materials, outcomes and challenges. Acta Biomater. 7, 1-15 (2011).
5. T. D. Johnson, K. L. Christman, Injectable hydrogel therapies and their delivery strategies for treating myocardial infarction. Expert Opin. Drug Deliv. 10, 59-72 (2012).
6. K. L. Christman, Treating the leading killer. Sci. Transl. Med. 4, 146fs26 (2012).
7. J.M. Singelyn, J. A. DeQuach, S. B. Seif-Naraghi, R. B. Littlefield, P. J. Schup-Magoffin, K. L. Christman, Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials 30, 5409-5416 (2009).
8. J. M. Singelyn, P. Sundaramurthy, T. D. Johnson, P. J. Schup-Magoffin, D. P. Hu, D. M. Faulk, J. Wang, K. M. Mayle, K. Bartels, M. Salvatore, A. M. Kinsey, A. N. Demaria, N. Dib, K. L. Christman, Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J. Am. Coll. Cardiol. 59, 751-763 (2012).
9. J. A. DeQuach, J. E. Lin, C. Cam, D. Hu, M. A. Salvatore, F. Sheikh, K. L. Christman, Injectable skeletal muscle matrix hydrogel promotes neovascularization and muscle cell infiltration in a hindlimb ischemia model. Eur. Cell. Mater. 23, 400-412 (2012).
10. J. E. Valentin, J. S. Badylak, G. P. McCabe, S. F. Badylak, Extracellular matrix bioscaffolds for orthopaedic applications. A comparative histologic study. J. Bone Joint Surg. Am. 88, 2673-2686 (2006).
11. K. A. Daly, A. M. Stewart-Akers, H. Hara, M. Ezzelarab, C. Long, K. Cordero, S. A. Johnson, D. Ayares, D. K. Cooper, S. F. Badylak, Effect of the aGal epitope on the response to small intestinal submucosa extracellular matrix in a nonhuman primate model. Tissue Eng. Part A 15, 3877-3888 (2009).
12. H. C. Ott, T. S. Matthiesen, S. K. Goh, L. D. Black, S. M. Kren, T. I. Netoff, D. A. Taylor, Perfusiondecellularized matrix: Using nature's platform to engineer a bioartificial heart. Nat. Med. 14, 213-221 (2008).
13. M. Okada, T. R. Payne, H. Oshima, N. Momoi, K. Tobita, J. Huard, Differential efficacy of gels derived from small intestinal submucosa as an injectable biomaterial for myocardial infarct repair. Biomaterials 31, 7678-7683 (2010).
14. S. B. Seif-Naraghi, D. Horn, P. A. Schup-Magoffin, K. L. Christman, Injectable extracellular matrix derived hydrogel provides a platform for enhanced retention and delivery of a heparin-binding growth factor. Acta Biomater. 8, 3695-3703 (2012).
15. J. A. DeQuach, V. Mezzano, A. Miglani, S. Lange, G. M. Keller, F. Sheikh, K. L. Christman, Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS One 5, e13039 (2010).
16. K. M. French, A. V. Boopathy, J. A. DeQuach, L. Chingozha, H. Lu, K. L. Christman, M. E. Davis, A naturally derived cardiac extracellular matrix enhances cardiac progenitor cell behaviour in vitro. Acta Biomater. 8, 4357-4364 (2012).
17. H. Kubo, N. Jaleel, A. Kumarapeli, R. M. Berretta, G. Bratinov, X. Shan, H. Wang, S. R. Houser, K. B. Margulies, Increased cardiac myocyte progenitors in failing human hearts. Circulation 118, 649-657 (2008).
18. Y. D. Lin, C. Y. Luo, Y. N. Hu, M. L. Yeh, Y. C. Hsueh, M. Y. Chang, D. C. Tsai, J. N. Wang, M. J. Tang, E. I. Wei, M. L. Springer, P. C. Hsieh, Instructive nanofiber scaffolds with VEGF create a microenvironment for arteriogenesis and cardiac repair. Sci. Transl. Med. 4, 146ra109 (2012).
19. J. Leor, S. Tuvia, V. Guetta, F.Manczur, D. Castel, U. Willenz, O. Petneházy, N. Landa, M. S. Feinberg, E. Konen, O. Goitein, O. Tsur-Gang, M. Shaul, L. Klapper, S. Cohen, Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in swine. J. Am. Coll. Cardiol. 54, 1014-1023 (2009).
20. R. J. Laham, M. Rezaee, M. Post, F. W. Sellke, R. A. Braeckman, D. Hung, M. Simons, Intracoronary and intravenous administration of basic fibroblast growth factor: Myocardial and tissue distribution. Drug Metab. Dispos. 27, 821-826 (1999).
21. R. J. Laham, N. A. Chronos, M. Pike, M. E. Leimbach, J. E. Udelson, J. D. Pearlman, R. I. Pettigrew, M. J. Whitehouse, C. Yoshizawa,M. Simons, Intracoronary basic fibroblast growth factor (FGF-2) in patients with severe ischemic heart disease: Results of a phase I open-label dose escalation study. J. Am. Coll. Cardiol. 36, 2132-2139 (2000).
22. K. Krause, K. Jaquet, C. Schneider, S. Haupt, M. V. Lioznov, K. M. Otte, K. H. Kuck, Percutaneous intramyocardial stem cell injection in patients with acute myocardial infarction: First-in-man study. Heart 95, 1145-1152 (2009).
23. K. E. Szummer, S. D. Solomon, E. J. Velazquez, R. Kilaru, J. McMurray, J. L. Rouleau, K. W. Mahaffey, A. P. Maggioni, R. M. Califf, M. A. Pfeffer, H. D. White; VALIANT Registry, Heart failure on admission and the risk of stroke following acute myocardial infarction: The VALIANT registry. Eur. Heart J. 26, 2114-2119 (2005).
24. E. J. Velazquez, M. A. Pfeffer, J. V. McMurray, A. P. Maggioni, J. L. Rouleau, F. Van de Werf, L. Kober, H. D. White, K. Swedberg, J. D. Leimberger, P. Gallo, M. A. Sellers, S. Edwards, M. Henis, R. M. Califf; VALIANT Investigators, VALsartan In Acute myocardial iNfarcTion (VALIANT) trial: Baseline characteristics in context. Eur. J. Heart Fail. 5, 537-544 (2003).
25. R. Mukherjee, J. A. Zavadzkas, S. M. Saunders, J. E. McLean, L. B. Jeffords, C. Beck, R. E. Stroud, A. M. Leone, C. N. Koval, W. T. Rivers, S. Basu, A. Sheehy, G. Michal, F. G. Spinale, Targeted myocardial microinjections of a biocomposite material reduces infarct expansion in pigs. Ann. Thorac. Surg. 86, 1268-1276 (2008).
26. J. L. Ifkovits, E. Tous, M. Minakawa, M. Morita, J. D. Robb, K. J. Koomalsingh, J. H. Gorman III, R. C. Gorman, J. A. Burdick, Injectable hydrogel properties influence infarct expansion and extent of postinfarction left ventricular remodeling in an ovine model. Proc. Natl. Acad. Sci. U.S.A. 107, 11507-11512 (2010).
27. Y. D. Lin, M. L. Yeh, Y. J. Yang, D. C. Tsai, T. Y. Chu, Y. Y. Shih, M. Y. Chang, Y. W. Liu, A. C. Tang, T. Y. Chen, C. Y. Luo, K. C. Chang, J. H. Chen, H. L. Wu, T. K. Hung, P. C. Hsieh, Intramyocardial peptide nanofiber injection improves postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs. Circulation 122, S132-S141 (2010).
28. B. N. Brown, J. E. Valentin, A. M. Stewart-Akers, G. P. McCabe, S. F. Badylak, Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30, 1482-1491 (2009).
29. S. F. Badylak, D. O. Freytes, T. W. Gilbert, Extracellular matrix as a biological scaffold material: Structure and function. Acta Biomater. 5, 1-13 (2009).
30. K. L. Fujimoto, Z. Ma, D. M. Nelson, R. Hashizume, J. Guan, K. Tobita, W. R. Wagner, Synthesis, characterization and therapeutic efficacy of a biodegradable, thermoresponsive hydrogel designed for application in chronic infarcted myocardium. Biomaterials 30, 4357-4368 (2009).
31. N. Dib, A. Campbell, D. B. Jacoby, A. Zawadzka, J. Ratliff, B. M. Miedzybrocki, A. Gahremanpour, E. B. Diethrich, S. R. Opie, Safety and feasibility of percutaneous autologous skeletal myoblast transplantation in the coil-infarcted swine myocardium. J. Pharmacol. Toxicol. Methods 54, 71-77 (2006).
32. H. Hamamoto, J. H. Gorman III, L. P. Ryan, R. Hinmon, T. P. Martens, M. D. Schuster, T. Plappert, M. Kiupel, M. G. St John-Sutton, S. Itescu, R. C. Gorman, Allogeneic mesenchymal precursor cell therapy to limit remodeling after myocardial infarction: The effect of cell dosage. Ann. Thorac. Surg. 87, 794-801 (2009).
33. H. D. White, R. M. Norris, M. A. Brown, P. W. Brandt, R. M. Whitlock, C. J. Wild, Left ventricular end-systolic volume as the major determinant of survival after recovery from myocardial infarction. Circulation 76, 44-51 (1987).
34. D. D. McManus, S. J. Shah, M. R. Fabi, A. Rosen, M. A. Whooley, N. B. Schiller, Prognostic value of left ventricular end-systolic volume index as a predictor of heart failure hospitalization in stable coronary artery disease: Data from the Heart and Soul Study. J. Am. Soc. Echocardiogr. 22, 190-197 (2009).
35. N. Dib, E. B. Diethrich, A. Campbell, A. Gahremanpour, M. McGarry, S. R. Opie, A percutaneous swine model of myocardial infarction. J. Pharmacol. Toxicol. Methods 53, 256-263 (2006).
36. M. Gyöngyösi, N. Dib, Diagnostic and prognostic value of 3D NOGA mapping in ischemic heart disease. Nat. Rev. Cardiol. 8, 393-404 (2011).
37. K. L. Christman, A. J. Vardanian, Q. Fang, R. E. Sievers, H. H. Fok, R. J. Lee, Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J. Am. Coll. Cardiol. 44, 654-660 (2004).