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Therapeutic Use of Bioengineered Materials for Myocardial Infarction

  • Veronika Sedlakova
  • Marc Ruel
  • Erik J. SuuronenEmail author
Chapter

Abstract

Cardiovascular disease is a leading cause of worldwide mortality. Despite the success of current therapies for acute myocardial infarction (MI), many patients still suffer irreversible damage, and the prevalence of heart failure is growing. After MI, the extracellular matrix (ECM) of the damaged myocardium is modified to produce scar tissue. This remodeling reduces the efficacy of therapies and also hinders endogenous repair mechanisms. Therefore, a strategy to prevent adverse remodeling and provide a suitable ECM environment that supports cells, tissue repair and functional restoration may lead to a superior therapeutic outcome in MI patients. Bioengineered materials are an attractive approach for achieving this. Herein, we review current research on materials that can act as a biomimetic matrix for supporting cellular repair in the post-MI heart. We also examine how nanomaterials are being used to treat the damaged heart. Finally, we provide an overview of the breakthroughs and limitations of biomaterial therapies for cardiac repair.

Notes

Acknowledgements

This work was supported by a Collaborative Research Grant from the Canadian Institutes of Health Research (CIHR) and the Natural Sciences and Engineering Research Council (NSERC) (CPG-158280), and a CIHR operating grant (MOP-77536).

Disclosure

All authors have read and approved the final version.

References

  1. 1.
    WHO. Global health estimates 2016: deaths by cause, age, sex, by country and by region, 2000–2016. Geneva; 2018.Google Scholar
  2. 2.
    Steenbergen C, Frangogiannis NG. Ischemic heart disease, chap. 36. In: Hill JA, Olson EN, editors. Muscle. Boston/Waltham: Academic Press; 2012. p. 495–521.CrossRefGoogle Scholar
  3. 3.
    Waller DG, Sampson AP. Ischaemic heart disease, chap. 5. In: Waller DG, Sampson AP, editors. Medical pharmacology and therapeutics, 5th ed. Elsevier; 2018. p. 93–110.Google Scholar
  4. 4.
    WHO. International classification of diseases 11th revision. https://icd.who.int/. 21 Dec 2018.
  5. 5.
    Roth GA, Johnson C, Abajobir A, Abd-Allah F, Abera SF, Abyu G, Ahmed M, Aksut B, Alam T, Alam K, et al. Global, regional, and national burden of cardiovascular diseases for 10 causes, 1990 to 2015. J Am Coll Cardiol. 2017;70(1):1–25.Google Scholar
  6. 6.
    Reed GW, Rossi JE, Cannon CP. Acute myocardial infarction. The Lancet. 2017;389(10065):197–210.CrossRefGoogle Scholar
  7. 7.
    Savarese G, Lund LH. Global public health burden of heart failure. Card Fail Rev. 2017;3(1):7–11.CrossRefGoogle Scholar
  8. 8.
    Azad N, Lemay G. Management of chronic heart failure in the older population. J Geriatr Cardiol. 2014;11(4):329–37.Google Scholar
  9. 9.
    Bonacchi M, Harmelin G, Bugetti M, Sani G. Mechanical ventricular assistance as destination therapy for end-stage heart failure: has it become a first line therapy? Front Surg 2015;2(35).Google Scholar
  10. 10.
    Laflamme MA, Sebastian MM, Buetow BS. Cardiovascular, chap. 10. In: Treuting PM, Dintzis SM, editors. Comparative anatomy and histology. San Diego: Academic Press; 2012. p. 135–53.CrossRefGoogle Scholar
  11. 11.
    Jourdan-LeSaux C, Zhang J, Lindsey ML. Extracellular matrix roles during cardiac repair. Life Sci. 2010;87(13):391–400.CrossRefGoogle Scholar
  12. 12.
    Horn MA, Trafford AW. Aging and the cardiac collagen matrix: novel mediators of fibrotic remodelling. J Mol Cell Cardiol. 2016;93:175–85.CrossRefGoogle Scholar
  13. 13.
    LeGrice I, Pope A, Smaill B. The architecture of the heart: myocyte organization and the cardiac extracellular matrix. In: Villarreal FJ, editor. Interstitial fibrosis in heart failure. New York, NY: Springer; 2005. p. 3–21.Google Scholar
  14. 14.
    Shamhart PE, Meszaros JG. Non-fibrillar collagens: key mediators of post-infarction cardiac remodeling? J Mol Cell Cardiol. 2010;48(3):530–7.CrossRefGoogle Scholar
  15. 15.
    Zeltz C, Gullberg D. The integrin–collagen connection—a glue for tissue repair? J Cell Sci. 2016;129(4):653.CrossRefGoogle Scholar
  16. 16.
    Shattil SJ, Kim C, Ginsberg MH. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol. 2010;11:288.CrossRefGoogle Scholar
  17. 17.
    Xu J, Mosher D. Fibronectin and other adhesive glycoproteins. In: Mecham RP, editor. The extracellular matrix: an overview. Berlin, Heidelberg: Springer; 2011. p. 41–75.Google Scholar
  18. 18.
    Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol. 2010;48(3):504–11.CrossRefGoogle Scholar
  19. 19.
    Lindsey ML. MMP induction and inhibition in myocardial infarction. Heart Fail Rev. 2004;9(1):7–19.CrossRefGoogle Scholar
  20. 20.
    Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol. 2001;17(1):463–516.CrossRefGoogle Scholar
  21. 21.
    Prabhu SD, Frangogiannis NG. The biological basis for cardiac repair after myocardial infarction: from inflammation to fibrosis. Circ Res. 2016;119(1):91–112.CrossRefGoogle Scholar
  22. 22.
    Hodgkinson CP, Bareja A, Gomez JA, Dzau VJ. Emerging concepts in paracrine mechanisms in regenerative cardiovascular medicine and biology. Circ Res. 2016;118(1):95–107.CrossRefGoogle Scholar
  23. 23.
    Fu X, Khalil H, Kanisicak O, Boyer JG, Vagnozzi RJ, Maliken BD, Sargent MA, Prasad V, Valiente-Alandi I, Blaxall BC, et al. Specialized fibroblast differentiated states underlie scar formation in the infarcted mouse heart. J Clin Invest. 2018;128(5):2127–43.CrossRefGoogle Scholar
  24. 24.
    Wei S, Chow LT, Shum IO, Qin L, Sanderson JE. Left and right ventricular collagen type I/III ratios and remodeling post-myocardial infarction. J Card Fail. 1999;5(2):117–26.CrossRefGoogle Scholar
  25. 25.
    Sun Y, Weber KT. Infarct scar: a dynamic tissue. Cardiovasc Res. 2000;46(2):250–6.CrossRefGoogle Scholar
  26. 26.
    Mason C, Dunnill P. A brief definition of regenerative medicine. Regen Med. 2007;3(1):1–5.CrossRefGoogle Scholar
  27. 27.
    Vadakke-Madathil S, Chaudhry Hina W. Cardiac regeneration. Circ Res. 2018;123(1):24–6.CrossRefGoogle Scholar
  28. 28.
    Tzahor E, Poss KD. Cardiac regeneration strategies: staying young at heart. Science. 2017;356(6342):1035.CrossRefGoogle Scholar
  29. 29.
    Cambria E, Pasqualini FS, Wolint P, Günter J, Steiger J, Bopp A, Hoerstrup SP, Emmert MY. Translational cardiac stem cell therapy: advancing from first-generation to next-generation cell types. NPJ Regen Med. 2017;2(1):17.CrossRefGoogle Scholar
  30. 30.
    Hastings CL, Roche ET, Ruiz-Hernandez E, Schenke-Layland K, Walsh CJ, Duffy GP. Drug and cell delivery for cardiac regeneration. Adv Drug Deliv Rev. 2015;84:85–106.CrossRefGoogle Scholar
  31. 31.
    Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci. 2010;123(24):4195.CrossRefGoogle Scholar
  32. 32.
    Li Z, Masumoto H, Jo JI, Yamazaki K, Ikeda T, Tabata Y, Minatoya K. Sustained release of basic fibroblast growth factor using gelatin hydrogel improved left ventricular function through the alteration of collagen subtype in a rat chronic myocardial infarction model. Gen Thorac Cardiovasc Surg. 2018;66(11):641–7.CrossRefGoogle Scholar
  33. 33.
    Kumagai M, Minakata K, Masumoto H, Yamamoto M, Yonezawa A, Ikeda T, Uehara K, Yamazaki K, Ikeda T, Matsubara K, et al. A therapeutic angiogenesis of sustained release of basic fibroblast growth factor using biodegradable gelatin hydrogel sheets in a canine chronic myocardial infarction model. Heart Vessels. 2018;33(10):1251-7.CrossRefGoogle Scholar
  34. 34.
    Qu H, Xie B-D, Wu J, Lv B, Chuai J-B, Li J-Z, Cai J, Wu H, Jiang S-L, Leng X-P, et al. Improved left ventricular aneurysm repair with cell- and cytokine-seeded collagen patches. Stem Cells Int. 2018;2018:4717802.CrossRefGoogle Scholar
  35. 35.
    O’Neill HS, O’Sullivan J, Porteous N, Ruiz-Hernandez E, Kelly HM, O’Brien FJ, Duffy GP. A collagen cardiac patch incorporating alginate microparticles permits the controlled release of hepatocyte growth factor and insulin-like growth factor-1 to enhance cardiac stem cell migration and proliferation. J Tissue Eng Regen Med. 2018;12(1):e384–94.CrossRefGoogle Scholar
  36. 36.
    Pandey R, Velasquez S, Durrani S, Jiang M, Neiman M, Crocker JS, Benoit JB, Rubinstein J, Paul A, Ahmed RP. MicroRNA-1825 induces proliferation of adult cardiomyocytes and promotes cardiac regeneration post ischemic injury. Am J Transl Res. 2017;9(6):3120–37.Google Scholar
  37. 37.
    Wang LL, Liu Y, Chung JJ, Wang T, Gaffey AC, Lu M, Cavanaugh CA, Zhou S, Kanade R, Atluri P, et al. Local and sustained miRNA delivery from an injectable hydrogel promotes cardiomyocyte proliferation and functional regeneration after ischemic injury. Nat Biomed Eng. 2017;1:983–92.CrossRefGoogle Scholar
  38. 38.
    Monaghan MG, Holeiter M, Brauchle E, Layland SL, Lu Y, Deb A, Pandit A, Nsair A, Schenke-Layland K. Exogenous miR-29B delivery through a hyaluronan-based injectable system yields functional maintenance of the infarcted myocardium. Tissue Eng Part A. 2017;24(1–2):57–67.Google Scholar
  39. 39.
    Wang Y, Zhang J, Qin Z, Fan Z, Lu C, Chen B, Zhao J, Li X, Xiao F, Lin X, et al. Preparation of high bioactivity multilayered bone-marrow mesenchymal stem cell sheets for myocardial infarction using a 3D-dynamic system. Acta Biomater. 2018;72:182–95.CrossRefGoogle Scholar
  40. 40.
    Paul A, Hasan A, Kindi HA, Gaharwar AK, Rao VTS, Nikkhah M, Shin SR, Krafft D, Dokmeci MR, Shum-Tim D, et al. Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair. ACS Nano. 2014;8(8):8050–62.CrossRefGoogle Scholar
  41. 41.
    Purcell BP, Barlow SC, Perreault PE, Freeburg L, Doviak H, Jacobs J, Hoenes A, Zellars KN, Khakoo AY, Lee T, et al. Delivery of a matrix metalloproteinase-responsive hydrogel releasing TIMP-3 after myocardial infarction: effects on left ventricular remodeling. Am J Physiol Heart Circ Physiol. 2018;315(4):H814–25.CrossRefGoogle Scholar
  42. 42.
    Fan Z, Xu Z, Niu H, Gao N, Guan Y, Li C, Dang Y, Cui X, Liu XL, Duan Y, et al. An injectable oxygen release system to augment cell survival and promote cardiac repair following myocardial infarction. Sci Rep. 2018;8(1):1371.Google Scholar
  43. 43.
    Waters R, Alam P, Pacelli S, Chakravarti AR, Ahmed RPH, Paul A. Stem cell-inspired secretome-rich injectable hydrogel to repair injured cardiac tissue. Acta Biomater. 2018;69:95–106.CrossRefGoogle Scholar
  44. 44.
    Atala A. Tissue engineering and regenerative medicine: concepts for clinical application. Rejuvenation Res. 2004;7(1):15–31.CrossRefGoogle Scholar
  45. 45.
    Hasirci V, Yucel D. Polymers used in tissue engineering. In: Wnek GE, Bowlin GL, editors. Encyclopedia of biomaterials and biomedical engineering. New York: Informa Healthcare USA, Inc.; 2008. p. 2282–99.Google Scholar
  46. 46.
    Boland ED, Espy PG, Bowlin GL. Tissue engineering scaffolds. In: Wnek GE, Bowlin GL, editors. Encyclopedia of biomaterials and biomedical engineering. New York: Informa Healthcare USA, Inc.; 2008. p. 2828–37.Google Scholar
  47. 47.
    Jang J, Park H-J, Kim S-W, Kim H, Park JY, Na SJ, Kim HJ, Park MN, Choi SH, Park SH, et al. 3D printed complex tissue construct using stem cell-laden decellularized extracellular matrix bioinks for cardiac repair. Biomaterials. 2017;112:264–74.CrossRefGoogle Scholar
  48. 48.
    French KM, Somasuntharam I, Davis ME. Self-assembling peptide-based delivery of therapeutics for myocardial infarction. Adv Drug Deliv Rev. 2016;96:40–53.CrossRefGoogle Scholar
  49. 49.
    Norahan MH, Amroon M, Ghahremanzadeh R, Mahmoodi M, Baheiraei N. Electroactive graphene oxide-incorporated collagen assisting vascularization for cardiac tissue engineering. J Biomed Mater Res A. 2019;107(1):204–19.CrossRefGoogle Scholar
  50. 50.
    Hosoyama K, Ahumada M, McTiernan CD, Davis DR, Variola F, Ruel M, Liang W, Suuronen EJ, Alarcon EI. Nanoengineered electroconductive collagen-based cardiac patch for infarcted myocardium repair. ACS Appl Mater Interfaces. 2018;10(51):44668-77.CrossRefGoogle Scholar
  51. 51.
    Dvir T, Timko BP, Brigham MD, Naik SR, Karajanagi SS, Levy O, Jin H, Parker KK, Langer R, Kohane DS. Nanowired three-dimensional cardiac patches. Nat Nanotechnol. 2011;6(11):720–5.CrossRefGoogle Scholar
  52. 52.
    Sun H, Zhou J, Huang Z, Qu L, Lin N, Liang C, Dai R, Tang L, Tian F. Carbon nanotube-incorporated collagen hydrogels improve cell alignment and the performance of cardiac constructs. Int J Nanomed. 2017;12:3109–20.CrossRefGoogle Scholar
  53. 53.
    Sherrell PC, Cieślar-Pobuda A, Ejneby MS, Sammalisto L, Gelmi A, de Muinck E, Brask J, Łos MJ, Rafat M. Rational design of a conductive collagen heart patch. Macromol Biosci. 2017;17(7):1600446.CrossRefGoogle Scholar
  54. 54.
    Kai D, Prabhakaran MP, Jin G, Ramakrishna S. Biocompatibility evaluation of electrically conductive nanofibrous scaffolds for cardiac tissue engineering. J Mater Chem B. 2013;1(17):2305–14.CrossRefGoogle Scholar
  55. 55.
    He Y, Ye G, Song C, Li C, Xiong W, Yu L, Qiu X, Wang L. Mussel-inspired conductive nanofibrous membranes repair myocardial infarction by enhancing cardiac function and revascularization. Theranostics. 2018;8(18):5159–77.CrossRefGoogle Scholar
  56. 56.
    Dong R, Zhao X, Guo B, Ma PX. Self-healing conductive injectable hydrogels with antibacterial activity as cell delivery carrier for cardiac cell therapy. ACS Appl Mater Interfaces. 2016;8(27):17138–50.CrossRefGoogle Scholar
  57. 57.
    Bao R, Tan B, Liang S, Zhang N, Wang W, Liu W. A π-π conjugation-containing soft and conductive injectable polymer hydrogel highly efficiently rebuilds cardiac function after myocardial infarction. Biomaterials. 2017;122:63–71.CrossRefGoogle Scholar
  58. 58.
    Mihic A, Cui Z, Wu J, Vlacic G, Miyagi Y, Li S-H, Lu S, Sung H-W, Weisel Richard D, Li R-K. A conductive polymer hydrogel supports cell electrical signaling and improves cardiac function after implantation into myocardial infarct. Circulation. 2015;132(8):772–84.CrossRefGoogle Scholar
  59. 59.
    Saravanan S, Sareen N, Abu-El-Rub E, Ashour H, Sequiera GL, Ammar HI, Gopinath V, Shamaa AA, Sayed SSE, Moudgil M, et al. Graphene oxide-gold nanosheets containing chitosan scaffold improves ventricular contractility and function after implantation into infarcted heart. Sci Rep. 2018;8(1):15069.Google Scholar
  60. 60.
    Kapnisi M, Mansfield C, Marijon C, Guex AG, Perbellini F, Bardi I, Humphrey EJ, Puetzer JL, Mawad D, Koutsogeorgis DC, et al. Auxetic cardiac patches with tunable mechanical and conductive properties toward treating myocardial infarction. Adv Funct Mater. 2018;28(21):1800618.CrossRefGoogle Scholar
  61. 61.
    Zhou J, Yang X, Liu W, Wang C, Shen Y, Zhang F, Zhu H, Sun H, Chen J, Lam J, et al. Injectable OPF/graphene oxide hydrogels provide mechanical support and enhance cell electrical signaling after implantation into myocardial infarct. Theranostics. 2018;8(12):3317–30.CrossRefGoogle Scholar
  62. 62.
    Christman KL, Lee RJ. Biomaterials for the treatment of myocardial infarction. J Am Coll Cardiol. 2006;48(5):907–13.CrossRefGoogle Scholar
  63. 63.
    Domenech M, Polo-Corrales L, Ramirez-Vick JE, Freytes DO. Tissue engineering strategies for myocardial regeneration: acellular versus cellular scaffolds? Tissue Eng Part B Rev. 2016;22(6):438–58.CrossRefGoogle Scholar
  64. 64.
    Ye L, Zimmermann W-H, Garry Daniel J, Zhang J. Patching the heart. Circ Res. 2013;113(7):922–32.CrossRefGoogle Scholar
  65. 65.
    Wang Q-l, Wang H-j, Li Z-h, Wang Y-l, Wu X-p, Tan Y-z. Mesenchymal stem cell-loaded cardiac patch promotes epicardial activation and repair of the infarcted myocardium. J Cell Mol Med. 2017;21(9):1751–66.CrossRefGoogle Scholar
  66. 66.
    Suarez SL, Rane AA, Muñoz A, Wright AT, Zhang SX, Braden RL, Almutairi A, McCulloch AD, Christman KL. Intramyocardial injection of hydrogel with high interstitial spread does not impact action potential propagation. Acta Biomater. 2015;26:13–22.CrossRefGoogle Scholar
  67. 67.
    Qiu Y, Hamilton SK, Temenoff J. Improving mechanical properties of injectable polymers and composites, chap. 4. In: Vernon B, editor. Injectable biomaterials. Woodhead Publishing; 2011. p. 61–91.Google Scholar
  68. 68.
    Lakshmanan R, Kumaraswamy P, Krishnan UM, Sethuraman S. Engineering a growth factor embedded nanofiber matrix niche to promote vascularization for functional cardiac regeneration. Biomaterials. 2016;97:176–95.CrossRefGoogle Scholar
  69. 69.
    Sadtler K, Singh A, Wolf MT, Wang X, Pardoll DM, Elisseeff JH. Design, clinical translation and immunological response of biomaterials in regenerative medicine. Nat Rev Mater. 2016;1:16040.CrossRefGoogle Scholar
  70. 70.
    Drury JL, Mooney DJ. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials. 2003;24(24):4337–51.CrossRefGoogle Scholar
  71. 71.
    Lee JH. Injectable hydrogels delivering therapeutic agents for disease treatment and tissue engineering. Biomater Res. 2018;22(1):27.CrossRefGoogle Scholar
  72. 72.
    Lee KY, Mooney DJ. Hydrogels for tissue engineering. Chem Rev. 2001;101(7):1869–80.CrossRefGoogle Scholar
  73. 73.
    Rodell CB, Kaminski AL, Burdick JA. Rational design of network properties in guest-host assembled and shear-thinning hyaluronic acid hydrogels. Biomacromolecules. 2013;14(11):4125–34.CrossRefGoogle Scholar
  74. 74.
    Rodell CB, MacArthur JW Jr, Dorsey SM, Wade RJ, Wang LL, Woo YJ, Burdick JA. Shear-thinning supramolecular hydrogels with secondary autonomous covalent crosslinking to modulate viscoelastic properties in vivo. Adv Funct Mater. 2015;25(4):636–44.CrossRefGoogle Scholar
  75. 75.
    Wong Po Foo CTS, Lee JS, Mulyasasmita W, Parisi-Amon A, Heilshorn SC. Two-component protein-engineered physical hydrogels for cell encapsulation. PNAS 2009;106(52):22067–72.CrossRefGoogle Scholar
  76. 76.
    Lu HD, Charati MB, Kim IL, Burdick JA. Injectable shear-thinning hydrogels engineered with a self-assembling Dock-and-Lock mechanism. Biomaterials. 2012;33(7):2145–53.CrossRefGoogle Scholar
  77. 77.
    Liu Y, Hsu S-h. Synthesis and biomedical applications of self-healing hydrogels. Front Chem. 2018;6(449).Google Scholar
  78. 78.
    Lindsey ML, Bolli R, Canty JM Jr, Du X-J, Frangogiannis NG, Frantz S, Gourdie RG, Holmes JW, Jones SP, Kloner RA, et al. Guidelines for experimental models of myocardial ischemia and infarction. Am J Physiol Heart Circ Physiol. 2018;314(4):H812–38.CrossRefGoogle Scholar
  79. 79.
    Naderi H, Matin MM, Bahrami AR. Review paper: critical issues in tissue engineering: biomaterials, cell sources, angiogenesis, and drug delivery systems. J Biomater Appl. 2011;26(4):383–417.CrossRefGoogle Scholar
  80. 80.
    Nair LS, Laurencin CT. Biodegradable polymers as biomaterials. Prog Polym Sci. 2007;32(8):762–98.CrossRefGoogle Scholar
  81. 81.
    Wang T, Lew J, Premkumar J, Poh CL, Naing MW. Production of recombinant collagen: state of the art and challenges. Eng Biol. 2017;1(1):18–23.CrossRefGoogle Scholar
  82. 82.
    Blackburn NJR, Sofrenovic T, Kuraitis D, Ahmadi A, McNeill B, Deng C, Rayner KJ, Zhong Z, Ruel M, Suuronen EJ. Timing underpins the benefits associated with injectable collagen biomaterial therapy for the treatment of myocardial infarction. Biomaterials. 2015;39:182–92.CrossRefGoogle Scholar
  83. 83.
    Serpooshan V, Zhao M, Metzler SA, Wei K, Shah PB, Wang A, Mahmoudi M, Malkovskiy AV, Rajadas J, Butte MJ, et al. The effect of bioengineered acellular collagen patch on cardiac remodeling and ventricular function post myocardial infarction. Biomaterials. 2013;34(36):9048–55.CrossRefGoogle Scholar
  84. 84.
    Dai W, Wold LE, Dow JS, Kloner RA. Thickening of the infarcted wall by collagen injection improves left ventricular function in rats: a novel approach to preserve cardiac function after myocardial infarction. J Am Coll Cardiol. 2005;46(4):714–9.CrossRefGoogle Scholar
  85. 85.
    Joshi J, Brennan D, Beachley V, Kothapalli CR. Cardiomyogenic differentiation of human bone marrow-derived mesenchymal stem cell spheroids within electrospun collagen nanofiber mats. J Biomed Mater Res A. 2018;106(12):3303–12.CrossRefGoogle Scholar
  86. 86.
    Valarmathi MT, Fuseler JW, Davis JM, Price RL. A novel human tissue-engineered 3-D functional vascularized cardiac muscle construct. Front Cell Dev Biol. 2017;5(2).Google Scholar
  87. 87.
    Ahmadi A, McNeill B, Vulesevic B, Kordos M, Mesana L, Thorn S, Renaud JM, Manthorp E, Kuraitis D, Toeg H, et al. The role of integrin α2 in cell and matrix therapy that improves perfusion, viability and function of infarcted myocardium. Biomaterials. 2014;35(17):4749–58.CrossRefGoogle Scholar
  88. 88.
    Giordano C, Thorn Stephanie L, Renaud Jennifer M, Al-Atassi T, Boodhwani M, Klein R, Kuraitis D, Dwivedi G, Zhang P, DaSilva Jean N, et al. Preclinical evaluation of biopolymer-delivered circulating angiogenic cells in a swine model of hibernating myocardium. Circ Cardiovasc Imaging. 2013;6(6):982–91.Google Scholar
  89. 89.
    Xu G, Wang X, Deng C, Teng X, Suuronen EJ, Shen Z, Zhong Z. Injectable biodegradable hybrid hydrogels based on thiolated collagen and oligo(acryloyl carbonate)–poly(ethylene glycol)–oligo(acryloyl carbonate) copolymer for functional cardiac regeneration. Acta Biomater. 2015;15:55–64.CrossRefGoogle Scholar
  90. 90.
    Xia Y, Zhu K, Lai H, Lang M, Xiao Y, Lian S, Guo C, Wang C. Enhanced infarct myocardium repair mediated by thermosensitive copolymer hydrogel-based stem cell transplantation. Exp Biol Med (Maywood). 2015;240(5):593–600.CrossRefGoogle Scholar
  91. 91.
    Liu Y, Xu Y, Wang Z, Wen D, Zhang W, Schmull S, Li H, Chen Y, Xue S. Electrospun nanofibrous sheets of collagen/elastin/polycaprolactone improve cardiac repair after myocardial infarction. Am J Transl Res. 2016;8(4):1678–94.Google Scholar
  92. 92.
    Shafiq M, Zhang Y, Zhu D, Zhao Z, Kim D-H, Kim SH, Kong D. In situ cardiac regeneration by using neuropeptide substance P and IGF-1C peptide eluting heart patches. Regen Biomater. 2018;5(5):303–16.CrossRefGoogle Scholar
  93. 93.
    Reis LA, Chiu LL, Wu J, Feric N, Laschinger C, Momen A, Li R-K, Radisic M. Hydrogels with integrin-binding angiopoietin-1-derived peptide, QHREDGS, for treatment of acute myocardial infarction. Circ Heart Fail. 2015;8(2):333–41.Google Scholar
  94. 94.
    Hosoyama K, Ahumada M, McTiernan CD, Bejjani J, Variola F, Ruel M, Xu B, Liang W, Suuronen EJ, Alarcon EI. Multi-functional thermo-crosslinkable collagen-metal nanoparticle composites for tissue regeneration: nanosilver vs. nanogold. RSC Adv. 2017;7(75):47704–8.CrossRefGoogle Scholar
  95. 95.
    Chachques JC, Trainini JC, Lago N, Masoli OH, Barisani JL, Cortes-Morichetti M, Schussler O, Carpentier A. Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM clinical trial): one year follow-up. Cell Transplant. 2007;16(9):927–34.CrossRefGoogle Scholar
  96. 96.
    Latifi N, Asgari M, Vali H, Mongeau L. A tissue-mimetic nano-fibrillar hybrid injectable hydrogel for potential soft tissue engineering applications. Sci Rep. 2018;8(1):1047.CrossRefGoogle Scholar
  97. 97.
    Su K, Wang C. Recent advances in the use of gelatin in biomedical research. Biotechnol Lett. 2015;37(11):2139–45.CrossRefGoogle Scholar
  98. 98.
    Nakajima K, Fujita J, Matsui M, Tohyama S, Tamura N, Kanazawa H, Seki T, Kishino Y, Hirano A, Okada M, et al. Gelatin hydrogel enhances the engraftment of transplanted cardiomyocytes and angiogenesis to ameliorate cardiac function after myocardial infarction. PLoS One. 2015;10(7):e0133308.CrossRefGoogle Scholar
  99. 99.
    Zhou J, Chen J, Sun H, Qiu X, Mou Y, Liu Z, Zhao Y, Li X, Han Y, Duan C, et al. Engineering the heart: evaluation of conductive nanomaterials for improving implant integration and cardiac function. Sci Rep. 2014;4:3733.Google Scholar
  100. 100.
    Shin SR, Jung SM, Zalabany M, Kim K, Zorlutuna P, Kim Sb, Nikkhah M, Khabiry M, Azize M, Kong J, et al. Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS Nano. 2013;7(3):2369–80.CrossRefGoogle Scholar
  101. 101.
    Noshadi I, Hong S, Sullivan KE, Shirzaei Sani E, Portillo-Lara R, Tamayol A, Shin SR, Gao AE, Stoppel WL, Black Iii LD, et al. In vitro and in vivo analysis of visible light crosslinkable gelatin methacryloyl (GelMA) hydrogels. Biomater Sci. 2017;5(10):2093–105.CrossRefGoogle Scholar
  102. 102.
    Yang B, Yao F, Hao T, Fang W, Ye L, Zhang Y, Wang Y, Li J, Wang C. Development of electrically conductive double-network hydrogels via one-step facile strategy for cardiac tissue engineering. Adv Healthcare Mater. 2016;5:474–88.CrossRefGoogle Scholar
  103. 103.
    Wang W, Tao H, Zhao Y, Sun X, Tang J, Selomulya C, Tang J, Chen T, Wang Y, Shu M, et al. Implantable and biodegradable macroporous iron oxide frameworks for efficient regeneration and repair of infracted heart. Theranostics. 2017;7(7):1966–75.CrossRefGoogle Scholar
  104. 104.
    Chang M-Y, Huang T-T, Chen C-H, Cheng B, Hwang S-M, Hsieh PCH. Injection of human cord blood cells with hyaluronan improves postinfarction cardiac repair in pigs. Stem Cells Transl Med. 2016;5(1):56–66.CrossRefGoogle Scholar
  105. 105.
    Vu TD, Pal SN, Ti L-K, Martinez EC, Rufaihah AJ, Ling LH, Lee C-N, Richards AM, Kofidis T. An autologous platelet-rich plasma hydrogel compound restores left ventricular structure, function and ameliorates adverse remodeling in a minimally invasive large animal myocardial restoration model: a translational approach: Vu and Pal “myocardial repair: PRP, hydrogel and supplements”. Biomaterials. 2015;45:27–35.CrossRefGoogle Scholar
  106. 106.
    Rodell CB, Lee ME, Wang H, Takebayashi S, Takayama T, Kawamura T, Arkles JS, Dusaj NN, Dorsey SM, Witschey WRT, et al. Injectable shear-thinning hydrogels for minimally invasive delivery to infarcted myocardium to limit left ventricular remodeling. Circ Cardiovasc Interv. 2016;9(10):e004058.Google Scholar
  107. 107.
    Wang LL, Chung JJ, Li EC, Uman S, Atluri P, Burdick JA. Injectable and protease-degradable hydrogel for siRNA sequestration and triggered delivery to the heart. J Control Release. 2018;285:152–61.CrossRefGoogle Scholar
  108. 108.
    Chen CW, Wang LL, Zaman S, Gordon J, Arisi MF, Venkataraman CM, Chung JJ, Hung G, Gaffey AC, Spruce LA, et al. Sustained release of endothelial progenitor cell-derived extracellular vesicles from shear-thinning hydrogels improves angiogenesis and promotes function after myocardial infarction. Cardiovasc Res. 2018;114(7):1029–40.CrossRefGoogle Scholar
  109. 109.
    Fan Z, Fu M, Xu Z, Zhang B, Li Z, Li H, Zhou X, Liu X, Duan Y, Lin P-H, et al. Sustained release of a peptide-based matrix metalloproteinase-2 inhibitor to attenuate adverse cardiac remodeling and improve cardiac function following myocardial infarction. Biomacromolecules. 2017;18(9):2820–9.CrossRefGoogle Scholar
  110. 110.
    Wang W, Tan B, Chen J, Bao R, Zhang X, Liang S, Shang Y, Liang W, Cui Y, Fan G, et al. An injectable conductive hydrogel encapsulating plasmid DNA-eNOs and ADSCs for treating myocardial infarction. Biomaterials. 2018;160:69–81.CrossRefGoogle Scholar
  111. 111.
    Dorsey SM, McGarvey JR, Wang H, Nikou A, Arama L, Koomalsingh KJ, Kondo N, Gorman JH, Pilla JJ, Gorman RC, et al. MRI evaluation of injectable hyaluronic acid-based hydrogel therapy to limit ventricular remodeling after myocardial infarction. Biomaterials. 2015;69:65–75.CrossRefGoogle Scholar
  112. 112.
    Tang J, Vandergriff A, Wang Z, Hensley MT, Cores J, Allen TA, Dinh P-U, Zhang J, Caranasos TG, Cheng K. A regenerative cardiac patch formed by spray painting of biomaterials onto the heart. Tissue Eng Part C. 2017;23(3):146–55.CrossRefGoogle Scholar
  113. 113.
    Vallée J-P, Hauwel M, Lepetit-Coiffé M, Bei W, Montet-Abou K, Meda P, Gardier S, Zammaretti P, Kraehenbuehl TP, Herrmann F, et al. Embryonic stem cell-based cardiopatches improve cardiac function in infarcted rats. Stem Cells Transl Med. 2012;1(3):248–60.CrossRefGoogle Scholar
  114. 114.
    Xiong Q, Hill KL, Li Q, Suntharalingam P, Mansoor A, Wang X, Jameel MN, Zhang P, Swingen C, Kaufman DS, et al. A fibrin patch-based enhanced delivery of human embryonic stem cell-derived vascular cell transplantation in a porcine model of postinfarction left ventricular remodeling. Stem Cells. 2011;29(2):367–75.CrossRefGoogle Scholar
  115. 115.
    Bellamy V, Vanneaux V, Bel A, Nemetalla H, Emmanuelle Boitard S, Farouz Y, Joanne P, Perier M-C, Robidel E, Mandet C, et al. Long-term functional benefits of human embryonic stem cell-derived cardiac progenitors embedded into a fibrin scaffold. J Heart Lung Transplant. 2015;34(9):1198–207.CrossRefGoogle Scholar
  116. 116.
    Blondiaux E, Pidial L, Autret G, Rahmi G, Balvay D, Audureau E, Wilhelm C, Guerin CL, Bruneval P, Silvestre J-S, et al. Bone marrow-derived mesenchymal stem cell-loaded fibrin patches act as a reservoir of paracrine factors in chronic myocardial infarction. J Tissue Eng Regen Med. 2017;11(12):3417–27.CrossRefGoogle Scholar
  117. 117.
    Wendel JS, Ye L, Tao R, Zhang J, Zhang J, Kamp TJ, Tranquillo RT. Functional effects of a tissue-engineered cardiac patch from human induced pluripotent stem cell-derived cardiomyocytes in a rat infarct model. Stem Cells Transl Med. 2015;4(11):1324–32.CrossRefGoogle Scholar
  118. 118.
    Mattapally S, Zhu W, Fast VG, Gao L, Worley C, Kannappan R, Borovjagin AV, Zhang J. Spheroids of cardiomyocytes derived from human-induced pluripotent stem cells improve recovery from myocardial injury in mice. Am J Physiol Heart Circ Physiol. 2018;315(2):H327–39.CrossRefGoogle Scholar
  119. 119.
    Roura S, Gálvez-Montón C, Bayes-Genis A. Fibrin, the preferred scaffold for cell transplantation after myocardial infarction? An old molecule with a new life. J Tissue Eng Regen Med. 2017;11(8):2304–13.CrossRefGoogle Scholar
  120. 120.
    Higuchi A, Ku N-J, Tseng Y-C, Pan C-H, Li H-F, Kumar SS, Ling Q-D, Chang Y, Alarfaj AA, Munusamy MA, et al. Stem cell therapies for myocardial infarction in clinical trials: bioengineering and biomaterial aspects. Lab Invest. 2017;97:1167.CrossRefGoogle Scholar
  121. 121.
    Menasché P, Vanneaux V, Hagège A, Bel A, Cholley B, Cacciapuoti I, Parouchev A, Benhamouda N, Tachdjian G, Tosca L, et al. Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report. Eur Heart J. 2015;36(30):2011–7.CrossRefGoogle Scholar
  122. 122.
    Gao L, Gregorich Zachery R, Zhu W, Mattapally S, Oduk Y, Lou X, Kannappan R, Borovjagin Anton V, Walcott Gregory P, Pollard Andrew E, et al. Large cardiac muscle patches engineered from human induced-pluripotent stem cell-derived cardiac cells improve recovery from myocardial infarction in swine. Circulation. 2018;137(16):1712–30.CrossRefGoogle Scholar
  123. 123.
    Riemenschneider SB, Mattia DJ, Wendel JS, Schaefer JA, Ye L, Guzman PA, Tranquillo RT. Inosculation and perfusion of pre-vascularized tissue patches containing aligned human microvessels after myocardial infarction. Biomaterials. 2016;97:51–61.CrossRefGoogle Scholar
  124. 124.
    Morin KT, Dries-Devlin JL, Tranquillo RT. Engineered microvessels with strong alignment and high lumen density via cell-induced fibrin gel compaction and interstitial flow. Tissue Eng Part A. 2013;20(3–4):553–65.Google Scholar
  125. 125.
    Su T, Huang K, Daniele MA, Hensley MT, Young AT, Tang J, Allen TA, Vandergriff AC, Erb PD, Ligler FS, et al. Cardiac stem cell patch integrated with microengineered blood vessels promotes cardiomyocyte proliferation and neovascularization after acute myocardial infarction. ACS Appl Mater Interfaces. 2018;10(39):33088–96.CrossRefGoogle Scholar
  126. 126.
    Wang Z, Lee SJ, Cheng H-J, Yoo JJ, Atala A. 3D bioprinted functional and contractile cardiac tissue constructs. Acta Biomater. 2018;70:48–56.CrossRefGoogle Scholar
  127. 127.
    Rufaihah AJ, Johari NA, Vaibavi SR, Plotkin M, Di Thien DT, Kofidis T, Seliktar D. Dual delivery of VEGF and ANG-1 in ischemic hearts using an injectable hydrogel. Acta Biomater. 2017;48:58–67.CrossRefGoogle Scholar
  128. 128.
    Bearzi C, Gargioli C, Baci D, Fortunato O, Shapira-Schweitzer K, Kossover O, Latronico MVG, Seliktar D, Condorelli G, Rizzi R. PlGF-MMP9-engineered iPS cells supported on a PEG-fibrinogen hydrogel scaffold possess an enhanced capacity to repair damaged myocardium. Cell Death Dis. 2014;5(2):e1053.CrossRefGoogle Scholar
  129. 129.
    Spotnitz WD. Fibrin sealant: the only approved hemostat, sealant, and adhesive—a laboratory and clinical perspective. ISRN Surg. 2014;2014:203943.CrossRefGoogle Scholar
  130. 130.
    Ott HC, Matthiesen TS, Goh S-K, Black LD, Kren SM, Netoff TI, Taylor DA. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14:213.CrossRefGoogle Scholar
  131. 131.
    Wassenaar JW, Gaetani R, Garcia JJ, Braden RL, Luo CG, Huang D, DeMaria AN, Omens JH, Christman KL. Evidence for mechanisms underlying the functional benefits of a myocardial matrix hydrogel for post-MI treatment. J Am Coll Cardiol. 2016;67(9):1074–86.CrossRefGoogle Scholar
  132. 132.
    Sarig U, Sarig H, de-Berardinis E, Chaw S-Y, Nguyen EBV, Ramanujam VS, Thang VD, Al-Haddawi M, Liao S, Seliktar D, et al. Natural myocardial ECM patch drives cardiac progenitor based restoration even after scarring. Acta Biomater. 2016;44:209–20.CrossRefGoogle Scholar
  133. 133.
    Shah M, Kc P, Copeland KM, Liao J, Zhang G. A thin layer of decellularized porcine myocardium for cell delivery. Sci Rep. 2018;8(1):16206.CrossRefGoogle Scholar
  134. 134.
    Wang Q, Yang H, Bai A, Jiang W, Li X, Wang X, Mao Y, Lu C, Qian R, Guo F, et al. Functional engineered human cardiac patches prepared from nature’s platform improve heart function after acute myocardial infarction. Biomaterials. 2016;105:52–65.CrossRefGoogle Scholar
  135. 135.
    Kajbafzadeh AM, Tafti SHA, Khorramirouz R, Sabetkish S, Kameli SM, Orangian S, Rabbani S, Oveisi N, Golmohammadi M, Kashani Z. Evaluating the role of autologous mesenchymal stem cell seeded on decellularized pericardium in the treatment of myocardial infarction: an animal study. Cell Tissue Bank. 2017;18(4):527–38.CrossRefGoogle Scholar
  136. 136.
    Kameli SM, Khorramirouz R, Eftekharzadeh S, Fendereski K, Daryabari SS, Tavangar SM, Kajbafzadeh A-M. Application of tissue-engineered pericardial patch in rat models of myocardial infarction. J Biomed Mater Res A. 2018;106(10):2670–8.CrossRefGoogle Scholar
  137. 137.
    Wan L, Chen Y, Wang Z, Wang W, Schmull S, Dong J, Xue S, Imboden H, Li J. Human heart valve-derived scaffold improves cardiac repair in a murine model of myocardial infarction. Sci Rep. 2017;7:39988.CrossRefGoogle Scholar
  138. 138.
    Li N, Huang R, Zhang X, Xin Y, Li J, Huang Y, Cui W, Stoltz JF, Zhou Y, Kong Q. Stem cells cardiac patch from decellularized umbilical artery improved heart function after myocardium infarction. Biomed Mater Eng. 2017;28(s1):S87–94.Google Scholar
  139. 139.
    Toeg HD, Tiwari-Pandey R, Seymour R, Ahmadi A, Crowe S, Vulesevic B, Suuronen EJ, Ruel M. Injectable small intestine submucosal extracellular matrix in an acute myocardial infarction model. Ann Thorac Surg. 2013;96(5):1686–94.CrossRefGoogle Scholar
  140. 140.
    Sonnenberg SB, Rane AA, Liu CJ, Rao N, Agmon G, Suarez S, Wang R, Munoz A, Bajaj V, Zhang S, et al. Delivery of an engineered HGF fragment in an extracellular matrix-derived hydrogel prevents negative LV remodeling post-myocardial infarction. Biomaterials. 2015;45:56–63.CrossRefGoogle Scholar
  141. 141.
    Francis MP, Breathwaite E, Bulysheva AA, Varghese F, Rodriguez RU, Dutta S, Semenov I, Ogle R, Huber A, Tichy A-M, et al. Human placenta hydrogel reduces scarring in a rat model of cardiac ischemia and enhances cardiomyocyte and stem cell cultures. Acta Biomater. 2017;52:92–104.CrossRefGoogle Scholar
  142. 142.
    Mewhort HEM, Turnbull JD, Satriano A, Chow K, Flewitt JA, Andrei A-C, Guzzardi DG, Svystonyuk DA, White JA, Fedak PWM. Epicardial infarct repair with bioinductive extracellular matrix promotes vasculogenesis and myocardial recovery. J Heart Lung Transplant. 2016;35(5):661–70.CrossRefGoogle Scholar
  143. 143.
    Mewhort HEM, Svystonyuk DA, Turnbull JD, Teng G, Belke DD, Guzzardi DG, Park DS, Kang S, Hollenberg MD, Fedak PWM. Bioactive extracellular matrix scaffold promotes adaptive cardiac remodeling and repair. JACC Basic Transl Sci. 2017;2(4):450–64.CrossRefGoogle Scholar
  144. 144.
    Wang L, Meier EM, Tian S, Lei I, Liu L, Xian S, Lam MT, Wang Z. Transplantation of Isl1 + cardiac progenitor cells in small intestinal submucosa improves infarcted heart function. Stem Cell Res Ther. 2017;8(1):230.CrossRefGoogle Scholar
  145. 145.
    Soucy KG, Smith EF, Monreal G, Rokosh G, Keller BB, Yuan F, Matheny RG, Fallon AM, Lewis BC, Sherwood LC, et al. Feasibility study of particulate extracellular matrix (P-ECM) and left ventricular assist device (HVAD) therapy in chronic ischemic heart failure bovine model. ASAIO J. 2015;61(2):161–9.CrossRefGoogle Scholar
  146. 146.
    Calgary Uo. Epicardial infarct repair using CorMatrix®-ECM: clinical feasibility study (EIR). National Library of Medicine. https://www.clinicaltrials.gov/ct2/show/NCT02887768?term=NCT02887768&rank=1 (2016). Accessed 07 Jan 2019.
  147. 147.
    Singelyn JM, DeQuach JA, Seif-Naraghi SB, Littlefield RB, Schup-Magoffin PJ, Christman KL. Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials. 2009;30(29):5409–16.CrossRefGoogle Scholar
  148. 148.
    Singelyn JM, Sundaramurthy P, Johnson TD, Schup-Magoffin PJ, Hu DP, Faulk DM, Wang J, Mayle KM, Bartels K, Salvatore M, et al. Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J Am Coll Cardiol. 2012;59(8):751–63.CrossRefGoogle Scholar
  149. 149.
    Seif-Naraghi SB, Singelyn JM, Salvatore MA, Osborn KG, Wang JJ, Sampat U, Kwan OL, Strachan GM, Wong J, Schup-Magoffin PJ, et al. Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med. 2013;5(173):173ra25.CrossRefGoogle Scholar
  150. 150.
    Ventrix I. A phase I, open-label study of the effects of percutaneous administration of an extracellular matrix hydrogel, VentriGel, following myocardial infarction. National Library of Medicine. https://clinicaltrials.gov/ct2/show/NCT02305602?term=NCT02305602 (2015). Accessed 15 Feb 2019.
  151. 151.
    Zhu Y, Matsumura Y, Wagner WR. Ventricular wall biomaterial injection therapy after myocardial infarction: advances in material design, mechanistic insight and early clinical experiences. Biomaterials. 2017;129:37–53.CrossRefGoogle Scholar
  152. 152.
    Panda NC, Zuckerman ST, Mesubi OO, Rosenbaum DS, Penn MS, Donahue JK, Alsberg E, Laurita KR. Improved conduction and increased cell retention in healed MI using mesenchymal stem cells suspended in alginate hydrogel. J Interv Card Electrophysiol. 2014;41(2):117–27.CrossRefGoogle Scholar
  153. 153.
    Daskalopoulos EP, Vilaeti AD, Barka E, Mantzouratou P, Kouroupis D, Kontonika M, Tourmousoglou C, Papalois A, Pantos C, Blankesteijn WM, et al. Attenuation of post-infarction remodeling in rats by sustained myocardial growth hormone administration. Growth Factors 2015;33(4):250–8.CrossRefGoogle Scholar
  154. 154.
    Kontonika M, Barka E, Roumpi M, La Rocca V, Lekkas P, Daskalopoulos EP, Vilaeti AD, Baltogiannis GG, Vlahos AP, Agathopoulos S, et al. Prolonged intra-myocardial growth hormone administration ameliorates post-infarction electrophysiologic remodeling in rats. Growth Factors 2017;35(1):1–11.CrossRefGoogle Scholar
  155. 155.
    Fang R, Qiao S, Liu Y, Meng Q, Chen X, Song B, Hou X, Tian W. Sustained co-delivery of BIO and IGF-1 by a novel hybrid hydrogel system to stimulate endogenous cardiac repair in myocardial infarcted rat hearts. Int J Nanomed. 2015;10:4691–703.CrossRefGoogle Scholar
  156. 156.
    Rodness J, Mihic A, Miyagi Y, Wu J, Weisel RD, Li R-K. VEGF-loaded microsphere patch for local protein delivery to the ischemic heart. Acta Biomater. 2016;45:169–81.CrossRefGoogle Scholar
  157. 157.
    Singh RD, Hillestad ML, Livia C, Li M, Alekseev AE, Witt TA, Stalboerger PG, Yamada S, Terzic A, Behfar A. M3RNA drives targeted gene delivery in acute myocardial infarction. Tissue Eng Part A. 2018;25(1-2):145-58.CrossRefGoogle Scholar
  158. 158.
    Leor J, Tuvia S, Guetta V, Manczur F, Castel D, Willenz U, Petneházy Ö, Landa N, Feinberg MS, Konen E, et al. Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in swine. J Am Coll Cardiol. 2009;54(11):1014–23.CrossRefGoogle Scholar
  159. 159.
    Frey N, Linke A, Süselbeck T, Müller-Ehmsen J, Vermeersch P, Schoors D, Rosenberg M, Bea F, Tuvia S, Leor J. Intracoronary delivery of injectable bioabsorbable scaffold (IK-5001) to treat left ventricular remodeling after ST-elevation myocardial infarction. Circ Cardiovasc Interv. 2014;7(6):806–12.CrossRefGoogle Scholar
  160. 160.
    Rao SV, Zeymer U, Douglas PS, Al-Khalidi H, Liu J, Gibson CM, Harrison RW, Joseph DS, Heyrman R, Krucoff MW. A randomized, double-blind, placebo-controlled trial to evaluate the safety and effectiveness of intracoronary application of a novel bioabsorbable cardiac matrix for the prevention of ventricular remodeling after large ST-segment elevation myocardial infarction: rationale and design of the PRESERVATION I trial. Am Heart J. 2015;170(5):929–37.CrossRefGoogle Scholar
  161. 161.
    McCune C, McKavanagh P, Menown IBA. A review of the key clinical trials of 2015: results and implications. Cardiol Ther. 2016;5(2):109–32.CrossRefGoogle Scholar
  162. 162.
    Sabbah HN, Wang M, Gupta RC, Rastogi S, Ilsar I, Sabbah MS, Kohli S, Helgerson S, Lee RJ. Augmentation of left ventricular wall thickness with alginate hydrogel implants improves left ventricular function and prevents progressive remodeling in dogs with chronic heart failure. JACC Heart Fail. 2013;1(3):252–8.CrossRefGoogle Scholar
  163. 163.
    Lee LC, Wall ST, Klepach D, Ge L, Zhang Z, Lee RJ, Hinson A, Gorman JH, Gorman RC, Guccione JM. Algisyl-LVR™ with coronary artery bypass grafting reduces left ventricular wall stress and improves function in the failing human heart. Int J Cardiol. 2013;168(3):2022–8.CrossRefGoogle Scholar
  164. 164.
    Mann DL, Lee RJ, Coats AJS, Neagoe G, Dragomir D, Pusineri E, Piredda M, Bettari L, Kirwan B-A, Dowling R, et al. One-year follow-up results from AUGMENT-HF: a multicentre randomized controlled clinical trial of the efficacy of left ventricular augmentation with algisyl in the treatment of heart failure. Eur J Heart Fail. 2016;18(3):314–25.CrossRefGoogle Scholar
  165. 165.
    Henning RJ, Khan A, Jimenez E. Chitosan hydrogels significantly limit left ventricular infarction and remodeling and preserve myocardial contractility. J Surg Res. 2016;201(2):490–7.CrossRefGoogle Scholar
  166. 166.
    Xu B, Li Y, Deng B, Liu X, Wang L, Zhu Q-L. Chitosan hydrogel improves mesenchymal stem cell transplant survival and cardiac function following myocardial infarction in rats. Exp Ther Med. 2017;13(2):588–94.CrossRefGoogle Scholar
  167. 167.
    Hardy B, Battler A, Weiss C, Kudasi O, Raiter A. Therapeutic angiogenesis of mouse hind limb ischemia by novel peptide activating GRP78 receptor on endothelial cells. Biochem Pharmacol. 2008;75(4):891–9.CrossRefGoogle Scholar
  168. 168.
    Shu Y, Hao T, Yao F, Qian Y, Wang Y, Yang B, Li J, Wang C. RoY peptide-modified chitosan-based hydrogel to improve angiogenesis and cardiac repair under hypoxia. ACS Appl Mater Interfaces. 2015;7(12):6505–17.CrossRefGoogle Scholar
  169. 169.
    Chen J, Zhan Y, Wang Y, Han D, Tao B, Luo Z, Ma S, Wang Q, Li X, Fan L, et al. Chitosan/silk fibroin modified nanofibrous patches with mesenchymal stem cells prevent heart remodeling post-myocardial infarction in rats. Acta Biomater. 2018;80:154–68.Google Scholar
  170. 170.
    Wang X, Wang L, Wu Q, Bao F, Yang H, Qiu X, Chang J. Chitosan/calcium silicate cardiac patch stimulates cardiomyocyte activity and myocardial performance after infarction by synergistic effect of bioactive ions and aligned nanostructure. ACS Appl Mater Interfaces. 2018;11(1):1449-68.CrossRefGoogle Scholar
  171. 171.
    Cui Z, Ni NC, Wu J, Du GQ, He S, Yau TM, Weisel RD, Sung HW, Li RK. Polypyrrole-chitosan conductive biomaterial synchronizes cardiomyocyte contraction and improves myocardial electrical impulse propagation. Theranostics. 2018;8(10):2752–64.CrossRefGoogle Scholar
  172. 172.
    Koutsopoulos S. Self-assembling peptide nanofiber hydrogels in tissue engineering and regenerative medicine: progress, design guidelines, and applications. J Biomed Mater Res A. 2016;104(4):1002–16.CrossRefGoogle Scholar
  173. 173.
    Cui H, Webber MJ, Stupp SI. Self-assembly of peptide amphiphiles: from molecules to nanostructures to biomaterials. Biopolymers. 2010;94(1):1–18.CrossRefGoogle Scholar
  174. 174.
    Li H, Gao J, Shang Y, Hua Y, Ye M, Yang Z, Ou C, Chen M. Folic acid derived hydrogel enhances the survival and promotes therapeutic efficacy of iPS cells for acute myocardial infarction. ACS Appl Mater Interfaces. 2018;10(29):24459–68CrossRefGoogle Scholar
  175. 175.
    Ichihara Y, Kaneko M, Yamahara K, Koulouroudias M, Sato N, Uppal R, Yamazaki K, Saito S, Suzuki K. Self-assembling peptide hydrogel enables instant epicardial coating of the heart with mesenchymal stromal cells for the treatment of heart failure. Biomaterials. 2018;154:12–23.CrossRefGoogle Scholar
  176. 176.
    Boopathy AV, Martinez MD, Smith AW, Brown ME, García AJ, Davis ME. Intramyocardial delivery of notch ligand-containing hydrogels improves cardiac function and angiogenesis following infarction. Tissue Eng Part A. 2015;21(17–18):2315–22.CrossRefGoogle Scholar
  177. 177.
    Martínez-Ramos C, Rodríguez-Pérez E, Garnes MP, Chachques JC, Moratal D, Vallés-Lluch A, Monleón Pradas M. Design and assembly procedures for large-sized biohybrid scaffolds as patches for myocardial infarct. Tissue Eng Part C Methods. 2014;20(10):817–27.CrossRefGoogle Scholar
  178. 178.
    Lamboni L, Gauthier M, Yang G, Wang Q. Silk sericin: a versatile material for tissue engineering and drug delivery. Biotechnol Adv. 2015;33(8):1855–67.CrossRefGoogle Scholar
  179. 179.
    Song Y, Zhang C, Zhang J, Sun N, Huang K, Li H, Wang Z, Huang K, Wang L. An injectable silk sericin hydrogel promotes cardiac functional recovery after ischemic myocardial infarction. Acta Biomater. 2016;41:210–23.CrossRefGoogle Scholar
  180. 180.
    Malki M, Fleischer S, Shapira A, Dvir T. Gold nanorod-based engineered cardiac patch for suture-free engraftment by near IR. Nano Lett. 2018;18(7):4069–73.CrossRefGoogle Scholar
  181. 181.
    Rabbani S, Soleimani M, Imani M, Sahebjam M, Ghiaseddin A, Nassiri SM, Majd Ardakani J, Tajik Rostami M, Jalali A, Mousanassab B, et al. Regenerating heart using a novel compound and human Wharton jelly mesenchymal stem cells. Arch Med Res. 2017;48(3):228–37.CrossRefGoogle Scholar
  182. 182.
    Chow A, Stuckey DJ, Kidher E, Rocco M, Jabbour RJ, Mansfield CA, Darzi A, Harding SE, Stevens MM, Athanasiou T. Human induced pluripotent stem cell-derived cardiomyocyte encapsulating bioactive hydrogels improve rat heart function post myocardial infarction. Stem Cell Rep. 2017;9(5):1415–22.CrossRefGoogle Scholar
  183. 183.
    Melhem M, Jensen T, Reinkensmeyer L, Knapp L, Flewellyn J, Schook L. A hydrogel construct and fibrin-based glue approach to deliver therapeutics in a murine myocardial infarction model. J Vis Exp. 2015;100:e52562.Google Scholar
  184. 184.
    Rabbani S, Soleimani M, Sahebjam M, Imani M, Haeri A, Ghiaseddin A, Nassiri SM, Majd Ardakani J, Tajik Rostami M, Jalali A, et al. Simultaneous delivery of Wharton’s jelly mesenchymal stem cells and insulin-like growth factor-1 in acute myocardial infarction. Iran J Pharm Res. 2018;17(2):426–41.Google Scholar
  185. 185.
    Steele AN, Cai L, Truong VN, Edwards BB, Goldstone AB, Eskandari A, Mitchell AC, Marquardt LM, Foster AA, Cochran JR, et al. A novel protein-engineered hepatocyte growth factor analog released via a shear-thinning injectable hydrogel enhances post-infarction ventricular function. Biotechnol Bioeng. 2017;114(10):2379–89.CrossRefGoogle Scholar
  186. 186.
    Ciuffreda MC, Malpasso G, Chokoza C, Bezuidenhout D, Goetsch KP, Mura M, Pisano F, Davies NH, Gnecchi M. Synthetic extracellular matrix mimic hydrogel improves efficacy of mesenchymal stromal cell therapy for ischemic cardiomyopathy. Acta Biomater. 2018;70:71–83.CrossRefGoogle Scholar
  187. 187.
    Woodruff MA, Hutmacher DW. The return of a forgotten polymer—polycaprolactone in the 21st century. Prog Polym Sci. 2010;35(10):1217–56.CrossRefGoogle Scholar
  188. 188.
    Soler-Botija C, Bagó JR, Llucià-Valldeperas A, Vallés-Lluch A, Castells-Sala C, Martínez-Ramos C, Fernández-Muiños T, Chachques JC, Pradas MM, Semino CE, et al. Engineered 3D bioimplants using elastomeric scaffold, self-assembling peptide hydrogel, and adipose tissue-derived progenitor cells for cardiac regeneration. Am J Transl Res. 2014;6(3):291–301.Google Scholar
  189. 189.
    Chung T-W, Lo H-Y, Chou T-H, Chen J-H, Wang S-S. Promoting cardiomyogenesis of hBMSC with a forming self-assembly hBMSC microtissues/HA-GRGD/SF-PCL cardiac patch is mediated by the synergistic functions of HA-GRGD. Macromol Biosci. 2017;17(3):1600173.CrossRefGoogle Scholar
  190. 190.
    Zhu H, Jiang X, Li X, Hu M, Wan W, Wen Y, He Y, Zheng X. Intramyocardial delivery of VEGF165 via a novel biodegradable hydrogel induces angiogenesis and improves cardiac function after rat myocardial infarction. Heart Vessels. 2016;31(6):963–75.CrossRefGoogle Scholar
  191. 191.
    Zhu H, Li X, Yuan M, Wan W, Hu M, Wang X, Jiang X. Intramyocardial delivery of bFGF with a biodegradable and thermosensitive hydrogel improves angiogenesis and cardio-protection in infarcted myocardium. Exp Ther Med. 2017;14(4):3609–15.CrossRefGoogle Scholar
  192. 192.
    Zeng X, Zou L, Levine RA, Guerrero JL, Handschumacher MD, Sullivan SM, Braithwaite GJC, Stone JR, Solis J, Muratoglu OK, et al. Efficacy of polymer injection for ischemic mitral regurgitation: persistent reduction of mitral regurgitation and attenuation of left ventricular remodeling. JACC Cardiovasc Interv. 2015;8(2):355–63.Google Scholar
  193. 193.
    Tang J, Wang J, Huang K, Ye Y, Su T, Qiao L, Hensley MT, Caranasos TG, Zhang J, Gu Z, et al. Cardiac cell-integrated microneedle patch for treating myocardial infarction. Sci Adv. 2018;4(11):eaat9365.CrossRefGoogle Scholar
  194. 194.
    Jamaiyar A, Wan W, Ohanyan V, Enrick M, Janota D, Cumpston D, Song H, Stevanov K, Kolz CL, Hakobyan T, et al. Alignment of inducible vascular progenitor cells on a micro-bundle scaffold improves cardiac repair following myocardial infarction. Basic Res Cardiol. 2017;112(4):41.Google Scholar
  195. 195.
    Spadaccio C, Nappi F, De Marco F, Sedati P, Taffon C, Nenna A, Crescenzi A, Chello M, Trombetta M, Gambardella I, et al. Implantation of a poly-l-lactide GCSF-functionalized scaffold in a model of chronic myocardial infarction. J Cardiovasc Transl Res. 2017;10(1):47–65.CrossRefGoogle Scholar
  196. 196.
    Zhu Y, Wood NA, Fok K, Yoshizumi T, Park DW, Jiang H, Schwartzman DS, Zenati MA, Uchibori T, Wagner WR, et al. Design of a coupled thermoresponsive hydrogel and robotic system for postinfarct biomaterial injection therapy. Ann Thorac Surg. 2016;102(3):780–6.CrossRefGoogle Scholar
  197. 197.
    Zhu Y, Matsumura Y, Velayutham M, Foley LM, Hitchens TK, Wagner WR. Reactive oxygen species scavenging with a biodegradable, thermally responsive hydrogel compatible with soft tissue injection. Biomaterials. 2018;177:98–112.CrossRefGoogle Scholar
  198. 198.
    Yoshizumi T, Zhu Y, Jiang H, D’Amore A, Sakaguchi H, Tchao J, Tobita K, Wagner WR. Timing effect of intramyocardial hydrogel injection for positively impacting left ventricular remodeling after myocardial infarction. Biomaterials. 2016;83:182–93.CrossRefGoogle Scholar
  199. 199.
    Shiekh PA, Singh A, Kumar A. Oxygen-releasing antioxidant cryogel scaffolds with sustained oxygen delivery for tissue engineering applications. ACS Appl Mater Interfaces. 2018;10(22):18458–69.CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Veronika Sedlakova
    • 1
  • Marc Ruel
    • 1
  • Erik J. Suuronen
    • 1
    Email author
  1. 1.BEaTS Research Program, Division of Cardiac SurgeryUniversity of Ottawa Heart InstituteOttawaCanada

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