Skip to main content
SpringerLink
Log in

Extracellular matrix–based biomaterials for cardiac regeneration and repair

  • Published:
Heart Failure Reviews Aims and scope Submit manuscript

Abstract

The spectrum of ischemic heart diseases, encompassing acute myocardial infarction to heart failure, represents the leading cause of death worldwide. Although extensive progress in cardiovascular diagnoses and therapy has been made, the prevalence of the disease continues to increase. Cardiac regeneration has a promising perspective for the therapy of heart failure. Recently, extracellular matrix (ECM) has been shown to play an important role in cardiac regeneration and repair after cardiac injury. There is also evidence that the ECM could be directly used as a drug to promote cardiomyocyte proliferation and cardiac regeneration. Increasing evidence supports that applying ECM biomaterials to maintain heart function recovery is an important approach to apply the concept of cardiac regenerative medicine to clinical practice in the future. Here, we will introduce the essential role of cardiac ECM in cardiac regeneration and summarize the approaches of delivering ECM biomaterials to promote cardiac repair in this review.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Joseph P, Leong D, McKee M, Anand SS, Schwalm JD, Teo K et al (2017) Reducing the global burden of cardiovascular disease, part 1: the epidemiology and risk factors. Circ Res 121(6):677–694. https://doi.org/10.1161/circresaha.117.308903

    Article  CAS  PubMed  Google Scholar 

  2. Nabel EG, Braunwald E (2012) A tale of coronary artery disease and myocardial infarction. N Engl J Med 366(1):54–63. https://doi.org/10.1056/NEJMra1112570

    Article  CAS  PubMed  Google Scholar 

  3. Xin M, Olson EN, Bassel-Duby R (2013) Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat Rev Mol Cell Biol 14(8):529–541. https://doi.org/10.1038/nrm3619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bassat E, Mutlak YE, Genzelinakh A, Shadrin IY, Baruch Umansky K, Yifa O et al (2017) The extracellular matrix protein agrin promotes heart regeneration in mice. Nature 547(7662):179–184. https://doi.org/10.1038/nature22978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Eroglu E, Chien KR (2017) Heart regeneration 4.0: Matrix Medicine. Dev Cell 42(1):7–8. https://doi.org/10.1016/j.devcel.2017.06.017

    Article  CAS  PubMed  Google Scholar 

  6. Shiro Yui LA, Maimets M, Pedersen MT, Fordham RP, Hansen SL, Larsen HL, Guiu J, Alves MRP, Rundsten CF, Johansen JV, Li Y, Madsen CD, Nakamura T, Watanabe M, Nielsen OH, Schweiger PJ, Piccolo S, Jensen KB (2018) YAP/TAZ-dependent reprogramming of colonic epithelium links ECM remodeling to tissue regeneration. Cell Stem Cell 22(1):35–49 e7

    Article  Google Scholar 

  7. Fry CS, Kirby TJ, Kosmac K, McCarthy JJ, Peterson CA (2017) Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell 20(1):56–59. https://doi.org/10.1016/j.stem.2016.09.010

    Article  CAS  PubMed  Google Scholar 

  8. Kutys ML, Yamada KM (2014) An extracellular-matrix-specific GEF-GAP interaction regulates Rho GTPase crosstalk for 3D collagen migration. Nat Cell Biol 16(9):909–917. https://doi.org/10.1038/ncb3026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Rozario T, DeSimone DW (2010) The extracellular matrix in development and morphogenesis: a dynamic view. Dev Biol 341(1):126–140. https://doi.org/10.1016/j.ydbio.2009.10.026

    Article  CAS  Google Scholar 

  10. Frangogiannis NG (2017) The extracellular matrix in myocardial injury, repair, and remodeling. J Clin Invest 127(5):1600–1612. https://doi.org/10.1172/jci87491

    Article  PubMed  PubMed Central  Google Scholar 

  11. Karsdal MA, Nielsen SH, Leeming DJ, Langholm LL, Nielsen MJ, Manon-Jensen T et al (2017) The good and the bad collagens of fibrosis - their role in signaling and organ function. Adv Drug Deliv Rev 121:43–56. https://doi.org/10.1016/j.addr.2017.07.014

    Article  CAS  Google Scholar 

  12. Bashey RI, Martinez-Hernandez A, Jimenez SA (1992) Isolation, characterization, and localization of cardiac collagen type VI. Associations with other extracellular matrix components. Circ Res 70(5):1006–1017

    Article  CAS  Google Scholar 

  13. Jugdutt BI (2003) Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough? Circulation. 108(11):1395–1403. https://doi.org/10.1161/01.cir.0000085658.98621.49

    Article  PubMed  Google Scholar 

  14. Astrof S, Kirby A, Lindblad-Toh K, Daly M, Hynes RO (2007) Heart development in fibronectin-null mice is governed by a genetic modifier on chromosome four. Mech Dev 124(7-8):551–558. https://doi.org/10.1016/j.mod.2007.05.004

    Article  CAS  PubMed  Google Scholar 

  15. Snider P, Hinton RB, Moreno-Rodriguez RA, Wang J, Rogers R, Lindsley A et al (2008) Periostin is required for maturation and extracellular matrix stabilization of noncardiomyocyte lineages of the heart. Circ Res 102(7):752–760. https://doi.org/10.1161/circresaha.107.159517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sullivan KE, Quinn KP, Tang KM, Georgakoudi I, Black LD 3rd. (2014) Extracellular matrix remodeling following myocardial infarction influences the therapeutic potential of mesenchymal stem cells. Stem Cell Res Ther 5(1):14. https://doi.org/10.1186/scrt403

    Article  PubMed  PubMed Central  Google Scholar 

  17. Chen WC, Wang Z, Missinato MA, Park DW, Long DW, Liu HJ et al (2016) Decellularized zebrafish cardiac extracellular matrix induces mammalian heart regeneration. Sci Adv 2(11):e1600844. https://doi.org/10.1126/sciadv.1600844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mercer SE, Odelberg SJ, Simon HG (2013) A dynamic spatiotemporal extracellular matrix facilitates epicardial-mediated vertebrate heart regeneration. Dev Biol 382(2):457–469. https://doi.org/10.1016/j.ydbio.2013.08.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lindsey ML (2018) Assigning matrix metalloproteinase roles in ischaemic cardiac remodelling. Nat Rev Cardiol 15(8):471–479. https://doi.org/10.1038/s41569-018-0022-z

    Article  PubMed  PubMed Central  Google Scholar 

  20. Dobaczewski M, Bujak M, Zymek P, Ren G, Entman ML, Frangogiannis NG (2006) Extracellular matrix remodeling in canine and mouse myocardial infarcts. Cell Tissue Res 324(3):475–488. https://doi.org/10.1007/s00441-005-0144-6

    Article  CAS  PubMed  Google Scholar 

  21. Li L, Zhao Q, Kong W (2018) Extracellular matrix remodeling and cardiac fibrosis. Matrix Biol 68-69:490–506. https://doi.org/10.1016/j.matbio.2018.01.013

    Article  CAS  PubMed  Google Scholar 

  22. Ren G, Michael LH, Entman ML, Frangogiannis NG (2002) Morphological characteristics of the microvasculature in healing myocardial infarcts. J Histochem Cytochem 50(1):71–79. https://doi.org/10.1177/002215540205000108

    Article  CAS  PubMed  Google Scholar 

  23. Trueblood NA, Xie Z, Communal C, Sam F, Ngoy S, Liaw L et al (2001) Exaggerated left ventricular dilation and reduced collagen deposition after myocardial infarction in mice lacking osteopontin. Circ Res 88(10):1080–1087. https://doi.org/10.1161/hh1001.090842

    Article  CAS  PubMed  Google Scholar 

  24. Schellings MW, Vanhoutte D, Swinnen M, Cleutjens JP, Debets J, van Leeuwen RE et al (2009) Absence of SPARC results in increased cardiac rupture and dysfunction after acute myocardial infarction. J Exp Med 206(1):113–123. https://doi.org/10.1084/jem.20081244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Frangogiannis NG, Ren G, Dewald O, Zymek P, Haudek S, Koerting A et al (2005) Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation. 111(22):2935–2942. https://doi.org/10.1161/circulationaha.104.510354

    Article  CAS  PubMed  Google Scholar 

  26. Brockes JP (1997) Amphibian limb regeneration: rebuilding a complex structure. Science (New York, NY) 276(5309):81–87

    Article  CAS  Google Scholar 

  27. Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science (New York, NY) 298(5601):2188–2190. https://doi.org/10.1126/science.1077857

    Article  CAS  Google Scholar 

  28. Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN et al (2011) Transient regenerative potential of the neonatal mouse heart. Science (New York, NY) 331(6020):1078–1080. https://doi.org/10.1126/science.1200708

    Article  CAS  Google Scholar 

  29. Williams C, Quinn KP, Georgakoudi I, Black LD 3rd. (2014) Young developmental age cardiac extracellular matrix promotes the expansion of neonatal cardiomyocytes in vitro. Acta Biomater 10(1):194–204. https://doi.org/10.1016/j.actbio.2013.08.037

    Article  CAS  PubMed  Google Scholar 

  30. Wang J, Karra R, Dickson AL, Poss KD (2013) Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev Biol 382(2):427–435. https://doi.org/10.1016/j.ydbio.2013.08.012

    Article  CAS  PubMed  Google Scholar 

  31. Ieda M, Tsuchihashi T, Ivey KN, Ross RS, Hong TT, Shaw RM et al (2009) Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell 16(2):233–244. https://doi.org/10.1016/j.devcel.2008.12.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Wang WE, Li L, Xia X, Fu W, Liao Q, Lan C et al (2017) Dedifferentiation, proliferation, and redifferentiation of adult mammalian cardiomyocytes after ischemic injury. Circulation. 136(9):834–848. https://doi.org/10.1161/circulationaha.116.024307

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kuhn B, del Monte F, Hajjar RJ, Chang YS, Lebeche D, Arab S et al (2007) Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nat Med 13(8):962–969. https://doi.org/10.1038/nm1619

    Article  CAS  PubMed  Google Scholar 

  34. Lorts A, Schwanekamp JA, Elrod JW, Sargent MA, Molkentin JD (2009) Genetic manipulation of periostin expression in the heart does not affect myocyte content, cell cycle activity, or cardiac repair. Circ Res 104(1):e1–e7. https://doi.org/10.1161/circresaha.108.188649

    Article  CAS  PubMed  Google Scholar 

  35. Chen Z, Xie J, Hao H, Lin H, Wang L, Zhang Y et al (2017) Ablation of periostin inhibits post-infarction myocardial regeneration in neonatal mice mediated by the phosphatidylinositol 3 kinase/glycogen synthase kinase 3beta/cyclin D1 signalling pathway. Cardiovasc Res 113(6):620–632. https://doi.org/10.1093/cvr/cvx001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Gupta V, Grande-Allen KJ (2006) Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells. Cardiovasc Res 72(3):375–383. https://doi.org/10.1016/j.cardiores.2006.08.017

    Article  CAS  PubMed  Google Scholar 

  37. Yahalom-Ronen Y, Rajchman D, Sarig R, Geiger B, Tzahor E (2015) Reduced matrix rigidity promotes neonatal cardiomyocyte dedifferentiation, proliferation and clonal expansion. eLife. 4. https://doi.org/10.7554/eLife.07455

  38. Akhyari P, Fedak PW, Weisel RD, Lee TY, Verma S, Mickle DA et al (2002) Mechanical stretch regimen enhances the formation of bioengineered autologous cardiac muscle grafts. Circulation. 106(12 Suppl 1):I137–I142

    PubMed  Google Scholar 

  39. Birla RK, Huang YC, Dennis RG (2007) Development of a novel bioreactor for the mechanical loading of tissue-engineered heart muscle. Tissue Eng 13(9):2239–2248. https://doi.org/10.1089/ten.2006.0359

    Article  CAS  PubMed  Google Scholar 

  40. Canseco DC, Kimura W, Garg S, Mukherjee S, Bhattacharya S, Abdisalaam S et al (2015) Human ventricular unloading induces cardiomyocyte proliferation. J Am Coll Cardiol 65(9):892–900. https://doi.org/10.1016/j.jacc.2014.12.027

    Article  PubMed  PubMed Central  Google Scholar 

  41. Kong YP, Rioja AY, Xue X, Sun Y, Fu J, Putnam AJ (2018) A systems mechanobiology model to predict cardiac reprogramming outcomes on different biomaterials. Biomaterials. 181:280–292. https://doi.org/10.1016/j.biomaterials.2018.07.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Vagnozzi RJ, Maillet M, Sargent MA, Khalil H, Johansen AKZ, Schwanekamp JA et al (2020) An acute immune response underlies the benefit of cardiac stem cell therapy. Nature. 577(7790):405–409. https://doi.org/10.1038/s41586-019-1802-2

    Article  CAS  PubMed  Google Scholar 

  43. Bissell MJ, Aggeler J (1987) Dynamic reciprocity: how do extracellular matrix and hormones direct gene expression? Prog Clin Biol Res 249:251–262

    CAS  PubMed  Google Scholar 

  44. Pomeroy JE, Helfer A, Bursac N (2019) Biomaterializing the promise of cardiac tissue engineering. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2019.02.009

  45. Wang F, Guan J (2010) Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy. Adv Drug Deliv Rev 62(7-8):784–797. https://doi.org/10.1016/j.addr.2010.03.001

    Article  CAS  PubMed  Google Scholar 

  46. Radisic M, Christman KL (2013) Materials science and tissue engineering: repairing the heart. Mayo Clin Proc 88(8):884–898. https://doi.org/10.1016/j.mayocp.2013.05.003

    Article  CAS  PubMed  Google Scholar 

  47. Christman KL, Lee RJ (2006) Biomaterials for the treatment of myocardial infarction. J Am Coll Cardiol 48(5):907–913. https://doi.org/10.1016/j.jacc.2006.06.005

    Article  CAS  PubMed  Google Scholar 

  48. Zimmermann WH, Melnychenko I, Eschenhagen T (2004) Engineered heart tissue for regeneration of diseased hearts. Biomaterials. 25(9):1639–1647

    Article  CAS  Google Scholar 

  49. Reis LA, Chiu LL, Feric N, Fu L, Radisic M (2016) Biomaterials in myocardial tissue engineering. J Tissue Eng Regen Med 10(1):11–28. https://doi.org/10.1002/term.1944

    Article  CAS  PubMed  Google Scholar 

  50. Johnson TD, Braden RL, Christman KL (2014) Injectable ECM scaffolds for cardiac repair. Methods Mol Biol (Clifton, NJ) 1181:109–120. https://doi.org/10.1007/978-1-4939-1047-2_10

    Article  CAS  Google Scholar 

  51. Duan Y, Liu Z, O'Neill J, Wan LQ, Freytes DO, Vunjak-Novakovic G (2011) Hybrid gel composed of native heart matrix and collagen induces cardiac differentiation of human embryonic stem cells without supplemental growth factors. J Cardiovasc Transl Res 4(5):605–615. https://doi.org/10.1007/s12265-011-9304-0

    Article  PubMed  PubMed Central  Google Scholar 

  52. Segers VF, Lee RT (2011) Biomaterials to enhance stem cell function in the heart. Circ Res 109(8):910–922. https://doi.org/10.1161/circresaha.111.249052

    Article  CAS  PubMed  Google Scholar 

  53. Tiburcy M, Hudson JE, Balfanz P, Schlick S, Meyer T, Chang Liao ML et al (2017) Defined engineered human myocardium with advanced maturation for applications in heart failure modeling and repair. Circulation. 135(19):1832–1847. https://doi.org/10.1161/circulationaha.116.024145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hirt MN, Boeddinghaus J, Mitchell A, Schaaf S, Bornchen C, Muller C et al (2014) Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation. J Mol Cell Cardiol 74:151–161. https://doi.org/10.1016/j.yjmcc.2014.05.009

    Article  CAS  PubMed  Google Scholar 

  55. Nawroth JC, Scudder LL, Halvorson RT, Tresback J, Ferrier JP, Sheehy SP et al (2018) Automated fabrication of photopatterned gelatin hydrogels for organ-on-chips applications. Biofabrication. 10(2):025004. https://doi.org/10.1088/1758-5090/aa96de

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Shin SR, Jung SM, Zalabany M, Kim K, Zorlutuna P, Kim SB et al (2013) Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS Nano 7(3):2369–2380. https://doi.org/10.1021/nn305559j

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Gaetani R, Feyen DA, Verhage V, Slaats R, Messina E, Christman KL et al (2015) Epicardial application of cardiac progenitor cells in a 3D-printed gelatin/hyaluronic acid patch preserves cardiac function after myocardial infarction. Biomaterials. 61:339–348. https://doi.org/10.1016/j.biomaterials.2015.05.005

    Article  CAS  PubMed  Google Scholar 

  58. Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI et al (2008) Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med 14(2):213–221. https://doi.org/10.1038/nm1684

    Article  CAS  PubMed  Google Scholar 

  59. Robertson MJ, Dries-Devlin JL, Kren SM, Burchfield JS, Taylor DA (2014) Optimizing recellularization of whole decellularized heart extracellular matrix. PLoS One 9(2):e90406. https://doi.org/10.1371/journal.pone.0090406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Tondreau MY, Laterreur V, Gauvin R, Vallieres K, Bourget JM, Lacroix D et al (2015) Mechanical properties of endothelialized fibroblast-derived vascular scaffolds stimulated in a bioreactor. Acta Biomater 18:176–185. https://doi.org/10.1016/j.actbio.2015.02.026

    Article  CAS  PubMed  Google Scholar 

  61. Wang Z, Long DW, Huang Y, Chen WCW, Kim K, Wang Y (2019) Decellularized neonatal cardiac extracellular matrix prevents widespread ventricular remodeling in adult mammals after myocardial infarction. Acta Biomater 87:140–151. https://doi.org/10.1016/j.actbio.2019.01.062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Tang-Quan KR, Mehta NA, Sampaio LC, Taylor DA (2018) Whole cardiac tissue bioscaffolds. Adv Exp Med Biol 1098:85–114. https://doi.org/10.1007/978-3-319-97421-7_5

    Article  CAS  PubMed  Google Scholar 

  63. Daley MC, Fenn SL, Black LD 3rd. (2018) Applications of cardiac extracellular matrix in tissue engineering and regenerative medicine. Adv Exp Med Biol 1098:59–83. https://doi.org/10.1007/978-3-319-97421-7_4

    Article  CAS  PubMed  Google Scholar 

  64. Seo Y, Jung Y, Kim SH (2018) Decellularized heart ECM hydrogel using supercritical carbon dioxide for improved angiogenesis. Acta Biomater 67:270–281. https://doi.org/10.1016/j.actbio.2017.11.046

    Article  CAS  PubMed  Google Scholar 

  65. Shudo Y, Cohen JE, MacArthur JW, Goldstone AB, Otsuru S, Trubelja A et al (2015) A tissue-engineered chondrocyte cell sheet induces extracellular matrix modification to enhance ventricular biomechanics and attenuate myocardial stiffness in ischemic cardiomyopathy. Tissue Eng A 21(19-20):2515–2525. https://doi.org/10.1089/ten.TEA.2014.0155

    Article  CAS  Google Scholar 

  66. Lee KM, Kim H, Nemeno JG, Yang W, Yoon J, Lee S et al (2015) Natural cardiac extracellular matrix sheet as a biomaterial for cardiomyocyte transplantation. Transplant Proc 47(3):751–756. https://doi.org/10.1016/j.transproceed.2014.12.030

    Article  CAS  PubMed  Google Scholar 

  67. Ishii M, Shibata R, Shimizu Y, Yamamoto T, Kondo K, Inoue Y et al (2014) Multilayered adipose-derived regenerative cell sheets created by a novel magnetite tissue engineering method for myocardial infarction. Int J Cardiol 175(3):545–553. https://doi.org/10.1016/j.ijcard.2014.06.034

    Article  PubMed  Google Scholar 

  68. Yeh YC, Lee WY, Yu CL, Hwang SM, Chung MF, Hsu LW et al (2010) Cardiac repair with injectable cell sheet fragments of human amniotic fluid stem cells in an immune-suppressed rat model. Biomaterials. 31(25):6444–6453. https://doi.org/10.1016/j.biomaterials.2010.04.069

    Article  CAS  PubMed  Google Scholar 

  69. Wang CC, Chen CH, Lin WW, Hwang SM, Hsieh PC, Lai PH et al (2008) Direct intramyocardial injection of mesenchymal stem cell sheet fragments improves cardiac functions after infarction. Cardiovasc Res 77(3):515–524. https://doi.org/10.1093/cvr/cvm046

    Article  CAS  PubMed  Google Scholar 

  70. Bracaglia LG, Winston S, Powell DA, Fisher JP (2019) Synthetic polymer coatings diminish chronic inflammation risk in large ECM-based materials. J Biomed Mater Res A 107(3):494–504. https://doi.org/10.1002/jbm.a.36564

    Article  CAS  PubMed  Google Scholar 

  71. Guan J, Wang F, Li Z, Chen J, Guo X, Liao J et al (2011) The stimulation of the cardiac differentiation of mesenchymal stem cells in tissue constructs that mimic myocardium structure and biomechanics. Biomaterials. 32(24):5568–5580. https://doi.org/10.1016/j.biomaterials.2011.04.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Loke WK, Khor E, Wee A, Teoh SH, Chian KS (1996) Hybrid biomaterials based on the interaction of polyurethane oligomers with porcine pericardium. Biomaterials. 17(22):2163–2172

    Article  CAS  Google Scholar 

  73. Yang MC, Wang SS, Chou NK, Chi NH, Huang YY, Chang YL et al (2009) The cardiomyogenic differentiation of rat mesenchymal stem cells on silk fibroin-polysaccharide cardiac patches in vitro. Biomaterials. 30(22):3757–3765. https://doi.org/10.1016/j.biomaterials.2009.03.057

    Article  CAS  PubMed  Google Scholar 

  74. Zhang B, Xiao Y, Hsieh A, Thavandiran N, Radisic M (2011) Micro- and nanotechnology in cardiovascular tissue engineering. Nanotechnology. 22(49):494003. https://doi.org/10.1088/0957-4484/22/49/494003

    Article  PubMed  Google Scholar 

  75. Kim TG, Shin H, Lim DW (2012) Biomimetic scaffolds for tissue engineering. Adv Funct Mater 22(12):2446–2468. https://doi.org/10.1002/adfm.201103083

    Article  CAS  Google Scholar 

  76. Boffito M, Di Meglio F, Mozetic P, Giannitelli SM, Carmagnola I, Castaldo C et al (2018) Surface functionalization of polyurethane scaffolds mimicking the myocardial microenvironment to support cardiac primitive cells. PLoS One 13(7):e0199896. https://doi.org/10.1371/journal.pone.0199896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Kyburz KA, Anseth KS (2015) Synthetic mimics of the extracellular matrix: how simple is complex enough? Ann Biomed Eng 43(3):489–500. https://doi.org/10.1007/s10439-015-1297-4

    Article  PubMed  PubMed Central  Google Scholar 

  78. Frydrych M, Roman S, MacNeil S, Chen B (2015) Biomimetic poly(glycerol sebacate)/poly(l-lactic acid) blend scaffolds for adipose tissue engineering. Acta Biomater 18:40–49. https://doi.org/10.1016/j.actbio.2015.03.004

    Article  CAS  PubMed  Google Scholar 

  79. Neal RA, McClugage SG, Link MC, Sefcik LS, Ogle RC, Botchwey EA (2009) Laminin nanofiber meshes that mimic morphological properties and bioactivity of basement membranes. Tissue Eng C Methods 15(1):11–21. https://doi.org/10.1089/ten.tec.2007.0366

    Article  CAS  Google Scholar 

  80. Migliorini E, Thakar D, Sadir R, Pleiner T, Baleux F, Lortat-Jacob H et al (2014) Well-defined biomimetic surfaces to characterize glycosaminoglycan-mediated interactions on the molecular, supramolecular and cellular levels. Biomaterials. 35(32):8903–8915. https://doi.org/10.1016/j.biomaterials.2014.07.017

    Article  CAS  PubMed  Google Scholar 

  81. Hematti P (2018) Role of extracellular matrix in cardiac cellular therapies. Adv Exp Med Biol 1098:173–188. https://doi.org/10.1007/978-3-319-97421-7_9

    Article  CAS  PubMed  Google Scholar 

  82. Singelyn JM, DeQuach JA, Seif-Naraghi SB, Littlefield RB, Schup-Magoffin PJ, Christman KL (2009) Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials. 30(29):5409–5416. https://doi.org/10.1016/j.biomaterials.2009.06.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Wu WQ, Peng S, Song ZY, Lin S (2019) Collagen biomaterial for the treatment of myocardial infarction: an update on cardiac tissue engineering and myocardial regeneration. Drug Deliv Transl Res. https://doi.org/10.1007/s13346-019-00627-0

  84. Roura S, Galvez-Monton C, Bayes-Genis A (2017) Fibrin, the preferred scaffold for cell transplantation after myocardial infarction? An old molecule with a new life. J Tissue Eng Regen Med 11(8):2304–2313. https://doi.org/10.1002/term.2129

    Article  CAS  PubMed  Google Scholar 

  85. Rufaihah AJ, Seliktar D (2016) Hydrogels for therapeutic cardiovascular angiogenesis. Adv Drug Deliv Rev 96:31–39. https://doi.org/10.1016/j.addr.2015.07.003

    Article  CAS  PubMed  Google Scholar 

  86. Arenas-Herrera JE, Ko IK, Atala A, Yoo JJ (2013) Decellularization for whole organ bioengineering. Biomed Mater (Bristol, England) 8(1):014106. https://doi.org/10.1088/1748-6041/8/1/014106

    Article  CAS  Google Scholar 

  87. Keane TJ, Swinehart IT, Badylak SF (2015) Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance. Methods (San Diego, Calif) 84:25–34. https://doi.org/10.1016/j.ymeth.2015.03.005

    Article  CAS  Google Scholar 

  88. Taylor DA, Sampaio LC, Ferdous Z, Gobin AS, Taite LJ (2018) Decellularized matrices in regenerative medicine. Acta Biomater 74:74–89. https://doi.org/10.1016/j.actbio.2018.04.044

    Article  CAS  PubMed  Google Scholar 

  89. Spang MT, Christman KL (2018) Extracellular matrix hydrogel therapies: in vivo applications and development. Acta Biomater 68:1–14. https://doi.org/10.1016/j.actbio.2017.12.019

    Article  CAS  PubMed  Google Scholar 

  90. Badylak SF, Taylor D, Uygun K (2011) Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 13:27–53. https://doi.org/10.1146/annurev-bioeng-071910-124743

    Article  CAS  PubMed  Google Scholar 

  91. Bejleri D, Davis ME (2019) Decellularized extracellular matrix materials for cardiac repair and regeneration. Adv Healthc Mater 8(5):e1801217. https://doi.org/10.1002/adhm.201801217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Schenke-Layland K, Rofail F, Heydarkhan S, Gluck JM, Ingle NP, Angelis E et al (2009) The use of three-dimensional nanostructures to instruct cells to produce extracellular matrix for regenerative medicine strategies. Biomaterials. 30(27):4665–4675. https://doi.org/10.1016/j.biomaterials.2009.05.033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Alrefai MT, Murali D, Paul A, Ridwan KM, Connell JM, Shum-Tim D (2015) Cardiac tissue engineering and regeneration using cell-based therapy. Stem Cells Cloning 8:81–101. https://doi.org/10.2147/sccaa.s54204

    Article  PubMed  PubMed Central  Google Scholar 

  94. Sakaguchi K, Shimizu T, Okano T (2015) Construction of three-dimensional vascularized cardiac tissue with cell sheet engineering. J Control Release 205:83–88. https://doi.org/10.1016/j.jconrel.2014.12.016

    Article  CAS  PubMed  Google Scholar 

  95. Cyranoski D (2018) ‘Reprogrammed’ stem cells approved to mend human hearts for the first time. Nature. 557(7707):619–620. https://doi.org/10.1038/d41586-018-05278-8

    Article  CAS  PubMed  Google Scholar 

  96. Kawamura M, Miyagawa S, Fukushima S, Saito A, Miki K, Funakoshi S et al (2017) Enhanced therapeutic effects of human iPS cell derived-cardiomyocyte by combined cell-sheets with omental flap technique in porcine ischemic cardiomyopathy model. Sci Rep 7(1):8824. https://doi.org/10.1038/s41598-017-08869-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Shimizu T, Sekine H, Yamato M, Okano T (2009) Cell sheet-based myocardial tissue engineering: new hope for damaged heart rescue. Curr Pharm Des 15(24):2807–2814

    Article  CAS  Google Scholar 

  98. Matsuura K, Utoh R, Nagase K, Okano T (2014) Cell sheet approach for tissue engineering and regenerative medicine. J Control Release 190:228–239. https://doi.org/10.1016/j.jconrel.2014.05.024

    Article  CAS  PubMed  Google Scholar 

  99. Efraim Y, Sarig H, Cohen Anavy N, Sarig U, de Berardinis E, Chaw SY et al (2017) Biohybrid cardiac ECM-based hydrogels improve long term cardiac function post myocardial infarction. Acta Biomater 50:220–233. https://doi.org/10.1016/j.actbio.2016.12.015

    Article  CAS  PubMed  Google Scholar 

  100. Klouda L (2015) Thermoresponsive hydrogels in biomedical applications: a seven-year update. Eur J Pharm Biopharm 97(Pt B):338–349. https://doi.org/10.1016/j.ejpb.2015.05.017

    Article  CAS  PubMed  Google Scholar 

  101. Zhu J, Marchant RE (2011) Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Dev 8(5):607–626. https://doi.org/10.1586/erd.11.27

    Article  CAS  Google Scholar 

  102. Ravichandran R, Venugopal JR, Sundarrajan S, Mukherjee S, Ramakrishna S (2012) Minimally invasive cell-seeded biomaterial systems for injectable/epicardial implantation in ischemic heart disease. Int J Nanomedicine 7:5969–5994. https://doi.org/10.2147/ijn.s37575

    Article  PubMed  PubMed Central  Google Scholar 

  103. Lau HK, Kiick KL (2015) Opportunities for multicomponent hybrid hydrogels in biomedical applications. Biomacromolecules. 16(1):28–42. https://doi.org/10.1021/bm501361c

    Article  CAS  PubMed  Google Scholar 

  104. Rufaihah AJ, Vaibavi SR, Plotkin M, Shen J, Nithya V, Wang J et al (2013) Enhanced infarct stabilization and neovascularization mediated by VEGF-loaded PEGylated fibrinogen hydrogel in a rodent myocardial infarction model. Biomaterials. 34(33):8195–8202. https://doi.org/10.1016/j.biomaterials.2013.07.031

    Article  CAS  PubMed  Google Scholar 

  105. Toba H, Lindsey ML (2019) Extracellular matrix roles in cardiorenal fibrosis: potential therapeutic targets for CVD and CKD in the elderly. Pharmacol Ther 193:99–120. https://doi.org/10.1016/j.pharmthera.2018.08.014

    Article  CAS  PubMed  Google Scholar 

  106. Yanamandala M, Zhu W, Garry DJ, Kamp TJ, Hare JM, Jun HW et al (2017) Overcoming the roadblocks to cardiac cell therapy using tissue engineering. J Am Coll Cardiol 70(6):766–775. https://doi.org/10.1016/j.jacc.2017.06.012

    Article  PubMed  PubMed Central  Google Scholar 

  107. Zhu Y, Matsumura Y, Wagner WR (2017) Ventricular wall biomaterial injection therapy after myocardial infarction: advances in material design, mechanistic insight and early clinical experiences. Biomaterials. 129:37–53. https://doi.org/10.1016/j.biomaterials.2017.02.032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Chien KR, Frisen J, Fritsche-Danielson R, Melton DA, Murry CE, Weissman IL (2019) Regenerating the field of cardiovascular cell therapy. Nat Biotechnol 37(3):232–237. https://doi.org/10.1038/s41587-019-0042-1

    Article  CAS  PubMed  Google Scholar 

  109. Kai D, Wang QL, Wang HJ, Prabhakaran MP, Zhang Y, Tan YZ et al (2014) Stem cell-loaded nanofibrous patch promotes the regeneration of infarcted myocardium with functional improvement in rat model. Acta Biomater 10(6):2727–2738. https://doi.org/10.1016/j.actbio.2014.02.030

    Article  CAS  PubMed  Google Scholar 

  110. Wendel JS, Ye L, Zhang P, Tranquillo RT, Zhang JJ (2014) Functional consequences of a tissue-engineered myocardial patch for cardiac repair in a rat infarct model. Tissue Eng A 20(7-8):1325–1335. https://doi.org/10.1089/ten.TEA.2013.0312

    Article  CAS  Google Scholar 

  111. Gaballa MA, Sunkomat JN, Thai H, Morkin E, Ewy G, Goldman S (2006) Grafting an acellular 3-dimensional collagen scaffold onto a non-transmural infarcted myocardium induces neo-angiogenesis and reduces cardiac remodeling. J Heart Lung Transplant 25(8):946–954. https://doi.org/10.1016/j.healun.2006.04.008

    Article  PubMed  Google Scholar 

  112. Serpooshan V, Zhao M, Metzler SA, Wei K, Shah PB, Wang A et al (2013) The effect of bioengineered acellular collagen patch on cardiac remodeling and ventricular function post myocardial infarction. Biomaterials. 34(36):9048–9055. https://doi.org/10.1016/j.biomaterials.2013.08.017

    Article  CAS  PubMed  Google Scholar 

  113. Deng C, Zhang P, Vulesevic B, Kuraitis D, Li F, Yang AF et al (2010) A collagen-chitosan hydrogel for endothelial differentiation and angiogenesis. Tissue Eng A 16(10):3099–3109. https://doi.org/10.1089/ten.tea.2009.0504

    Article  CAS  Google Scholar 

  114. Slaughter BV, Khurshid SS, Fisher OZ, Khademhosseini A, Peppas NA (2009) Hydrogels in regenerative medicine. Adv Mater (Deerfield Beach, Fla) 21(32-33):3307–3329. https://doi.org/10.1002/adma.200802106

    Article  CAS  Google Scholar 

  115. Phelps EA, Enemchukwu NO, Fiore VF, Sy JC, Murthy N, Sulchek TA et al (2012) Maleimide cross-linked bioactive PEG hydrogel exhibits improved reaction kinetics and cross-linking for cell encapsulation and in situ delivery. Adv Mater (Deerfield Beach, Fla) 24(1):64–70, 2. https://doi.org/10.1002/adma.201103574

    Article  CAS  Google Scholar 

  116. Saludas L, Pascual-Gil S, Prosper F, Garbayo E, Blanco-Prieto M (2017) Hydrogel based approaches for cardiac tissue engineering. Int J Pharm 523(2):454–475. https://doi.org/10.1016/j.ijpharm.2016.10.061

    Article  CAS  PubMed  Google Scholar 

  117. Annabi N, Tamayol A, Uquillas JA, Akbari M, Bertassoni LE, Cha C et al (2014) 25th anniversary article: Rational design and applications of hydrogels in regenerative medicine. Adv Mater (Deerfield Beach, Fla) 26(1):85–123

    Article  CAS  Google Scholar 

  118. Shi K, Wang YL, Qu Y, Liao JF, Chu BY, Zhang HP et al (2016) Synthesis, characterization, and application of reversible PDLLA-PEG-PDLLA copolymer thermogels in vitro and in vivo. Sci Rep 6:19077. https://doi.org/10.1038/srep19077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Vo TN, Ekenseair AK, Spicer PP, Watson BM, Tzouanas SN, Roh TT et al (2015) In vitro and in vivo evaluation of self-mineralization and biocompatibility of injectable, dual-gelling hydrogels for bone tissue engineering. J Control Release 205:25–34. https://doi.org/10.1016/j.jconrel.2014.11.028

    Article  CAS  PubMed  Google Scholar 

  120. Barnes AL, Genever PG, Rimmer S, Coles MC (2016) Collagen-poly(N-isopropylacrylamide) hydrogels with tunable properties. Biomacromolecules. 17(3):723–734. https://doi.org/10.1021/acs.biomac.5b01251

    Article  CAS  PubMed  Google Scholar 

  121. Das D, Ghosh P, Ghosh A, Haldar C, Dhara S, Panda AB et al (2015) Stimulus-responsive, biodegradable, biocompatible, covalently cross-linked hydrogel based on dextrin and poly(N-isopropylacrylamide) for in vitro/in vivo controlled drug release. ACS Appl Mater Interfaces 7(26):14338–14351. https://doi.org/10.1021/acsami.5b02975

    Article  CAS  PubMed  Google Scholar 

  122. Chen FM, Liu X (2016) Advancing biomaterials of human origin for tissue engineering. Prog Polym Sci 53:86–168. https://doi.org/10.1016/j.progpolymsci.2015.02.004

    Article  CAS  PubMed  Google Scholar 

  123. Hastings CL, Roche ET, Ruiz-Hernandez E, Schenke-Layland K, Walsh CJ, Duffy GP (2015) Drug and cell delivery for cardiac regeneration. Adv Drug Deliv Rev 84:85–106. https://doi.org/10.1016/j.addr.2014.08.006

    Article  CAS  PubMed  Google Scholar 

  124. Wang H, Zhou J, Liu Z, Wang C (2010) Injectable cardiac tissue engineering for the treatment of myocardial infarction. J Cell Mol Med 14(5):1044–1055. https://doi.org/10.1111/j.1582-4934.2010.01046.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Ungerleider JL, Johnson TD, Rao N, Christman KL (2015) Fabrication and characterization of injectable hydrogels derived from decellularized skeletal and cardiac muscle. Methods (San Diego, Calif) 84:53–59. https://doi.org/10.1016/j.ymeth.2015.03.024

    Article  CAS  Google Scholar 

  126. Shu Y, Hao T, Yao F, Qian Y, Wang Y, Yang B et al (2015) RoY peptide-modified chitosan-based hydrogel to improve angiogenesis and cardiac repair under hypoxia. ACS Appl Mater Interfaces 7(12):6505–6517. https://doi.org/10.1021/acsami.5b01234

    Article  CAS  PubMed  Google Scholar 

  127. Singelyn JM, Sundaramurthy P, Johnson TD, Schup-Magoffin PJ, Hu DP, Faulk DM et al (2012) Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J Am Coll Cardiol 59(8):751–763. https://doi.org/10.1016/j.jacc.2011.10.888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Sawa Y, Miyagawa S, Sakaguchi T, Fujita T, Matsuyama A, Saito A et al (2012) Tissue engineered myoblast sheets improved cardiac function sufficiently to discontinue LVAS in a patient with DCM: report of a case. Surg Today 42(2):181–184. https://doi.org/10.1007/s00595-011-0106-4

    Article  PubMed  Google Scholar 

  129. Nishida K, Yamato M, Hayashida Y, Watanabe K, Yamamoto K, Adachi E et al (2004) Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. N Engl J Med 351(12):1187–1196. https://doi.org/10.1056/NEJMoa040455

    Article  CAS  Google Scholar 

  130. Sato M, Yamato M, Hamahashi K, Okano T, Mochida J (2014) Articular cartilage regeneration using cell sheet technology. Anat Rec (Hoboken, NJ : 2007) 297(1):36–43. https://doi.org/10.1002/ar.22829

    Article  CAS  Google Scholar 

  131. Ohki T, Yamato M, Murakami D, Takagi R, Yang J, Namiki H et al (2006) Treatment of oesophageal ulcerations using endoscopic transplantation of tissue-engineered autologous oral mucosal epithelial cell sheets in a canine model. Gut. 55(12):1704–1710. https://doi.org/10.1136/gut.2005.088518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Itabashi Y, Miyoshi S, Yuasa S, Fujita J, Shimizu T, Okano T et al (2005) Analysis of the electrophysiological properties and arrhythmias in directly contacted skeletal and cardiac muscle cell sheets. Cardiovasc Res 67(3):561–570. https://doi.org/10.1016/j.cardiores.2005.03.014

    Article  CAS  PubMed  Google Scholar 

  133. Itabashi Y, Miyoshi S, Kawaguchi H, Yuasa S, Tanimoto K, Furuta A et al (2005) A new method for manufacturing cardiac cell sheets using fibrin-coated dishes and its electrophysiological studies by optical mapping. Artif Organs 29(2):95–103. https://doi.org/10.1111/j.1525-1594.2005.29020.x

    Article  PubMed  Google Scholar 

  134. Matsuura K, Wada M, Shimizu T, Haraguchi Y, Sato F, Sugiyama K et al (2012) Creation of human cardiac cell sheets using pluripotent stem cells. Biochem Biophys Res Commun 425(2):321–327. https://doi.org/10.1016/j.bbrc.2012.07.089

    Article  CAS  PubMed  Google Scholar 

  135. Lee P, Klos M, Bollensdorff C, Hou L, Ewart P, Kamp TJ et al (2012) Simultaneous voltage and calcium mapping of genetically purified human induced pluripotent stem cell-derived cardiac myocyte monolayers. Circ Res 110(12):1556–1563. https://doi.org/10.1161/circresaha.111.262535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Fujita J, Itabashi Y, Seki T, Tohyama S, Tamura Y, Sano M et al (2012) Myocardial cell sheet therapy and cardiac function. Am J Physiol Heart Circ Physiol 303(10):H1169–H1182. https://doi.org/10.1152/ajpheart.00376.2012

    Article  CAS  PubMed  Google Scholar 

  137. Galaup A, Gomez E, Souktani R, Durand M, Cazes A, Monnot C et al (2012) Protection against myocardial infarction and no-reflow through preservation of vascular integrity by angiopoietin-like 4. Circulation. 125(1):140–149. https://doi.org/10.1161/circulationaha.111.049072

    Article  CAS  PubMed  Google Scholar 

  138. Kofidis T, de Bruin JL, Hoyt G, Lebl DR, Tanaka M, Yamane T et al (2004) Injectable bioartificial myocardial tissue for large-scale intramural cell transfer and functional recovery of injured heart muscle. J Thorac Cardiovasc Surg 128(4):571–578. https://doi.org/10.1016/j.jtcvs.2004.05.021

    Article  PubMed  Google Scholar 

  139. Iyisoy A, Ozturk C, Celik T, Demirkol S, Cingoz F, Unlu M et al (2015) Percutaneous transapical closure of cardiac apex with an ADO-II device after successful transapical transcatheter prosthetic mitral paravalvular leak closure. Int J Cardiol 189:289–292. https://doi.org/10.1016/j.ijcard.2015.04.076

    Article  PubMed  Google Scholar 

  140. Wu KH, Liu YL, Zhou B, Han ZC (2006) Cellular therapy and myocardial tissue engineering: the role of adult stem and progenitor cells. Eur J Cardiothorac Surg 30(5):770–781. https://doi.org/10.1016/j.ejcts.2006.08.003

    Article  PubMed  Google Scholar 

  141. Aamodt JM, Grainger DW (2016) Extracellular matrix-based biomaterial scaffolds and the host response. Biomaterials. 86:68–82. https://doi.org/10.1016/j.biomaterials.2016.02.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Alvarez MM, Liu JC, Trujillo-de Santiago G, Cha BH, Vishwakarma A, Ghaemmaghami AM et al (2016) Delivery strategies to control inflammatory response: modulating M1-M2 polarization in tissue engineering applications. J Control Release 240:349–363. https://doi.org/10.1016/j.jconrel.2016.01.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Du C, Cui FZ, Zhu XD, de Groot K (1999) Three-dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture. J Biomed Mater Res 44(4):407–415

    Article  CAS  Google Scholar 

  144. Badylak SF (2007) The extracellular matrix as a biologic scaffold material. Biomaterials. 28(25):3587–3593. https://doi.org/10.1016/j.biomaterials.2007.04.043

    Article  CAS  PubMed  Google Scholar 

  145. Bouten CV, Dankers PY, Driessen-Mol A, Pedron S, Brizard AM, Baaijens FP (2011) Substrates for cardiovascular tissue engineering. Adv Drug Deliv Rev 63(4-5):221–241. https://doi.org/10.1016/j.addr.2011.01.007

    Article  CAS  PubMed  Google Scholar 

  146. Bracaglia LG, Fisher JP (2015) Extracellular matrix-based biohybrid materials for engineering compliant, matrix-dense tissues. Adv Healthc Mater 4(16):2475–2487. https://doi.org/10.1002/adhm.201500236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Mathur A, Ma Z, Loskill P, Jeeawoody S, Healy KE (2016) In vitro cardiac tissue models: current status and future prospects. Adv Drug Deliv Rev 96:203–213. https://doi.org/10.1016/j.addr.2015.09.011

    Article  CAS  PubMed  Google Scholar 

  148. Leor J, Amsalem Y, Cohen S (2005) Cells, scaffolds, and molecules for myocardial tissue engineering. Pharmacol Ther 105(2):151–163. https://doi.org/10.1016/j.pharmthera.2004.10.003

    Article  CAS  PubMed  Google Scholar 

  149. Berglund JD, Galis ZS (2003) Designer blood vessels and therapeutic revascularization. Br J Pharmacol 140(4):627–636. https://doi.org/10.1038/sj.bjp.0705457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Tedder ME, Liao J, Weed B, Stabler C, Zhang H, Simionescu A et al (2009) Stabilized collagen scaffolds for heart valve tissue engineering. Tissue Eng A 15(6):1257–1268. https://doi.org/10.1089/ten.tea.2008.0263

    Article  CAS  Google Scholar 

  151. Arts T, Bovendeerd PH, Prinzen FW, Reneman RS (1991) Relation between left ventricular cavity pressure and volume and systolic fiber stress and strain in the wall. Biophys J 59(1):93–102. https://doi.org/10.1016/s0006-3495(91)82201-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Mol A, van Lieshout MI, Dam-de Veen CG, Neuenschwander S, Hoerstrup SP, Baaijens FP et al (2005) Fibrin as a cell carrier in cardiovascular tissue engineering applications. Biomaterials. 26(16):3113–3121. https://doi.org/10.1016/j.biomaterials.2004.08.007

    Article  CAS  PubMed  Google Scholar 

  153. Langer R, Vacanti JP (1993) Tissue engineering. Science. 260(5110):920–926

    Article  CAS  Google Scholar 

  154. Fuchs JR, Nasseri BA, Vacanti JP (2001) Tissue engineering: a 21st century solution to surgical reconstruction. Ann Thorac Surg 72(2):577–591

    Article  CAS  Google Scholar 

  155. Ishii O, Shin M, Sueda T, Vacanti JP (2005) In vitro tissue engineering of a cardiac graft using a degradable scaffold with an extracellular matrix-like topography. J Thorac Cardiovasc Surg 130(5):1358–1363. https://doi.org/10.1016/j.jtcvs.2005.05.048

    Article  PubMed  Google Scholar 

  156. Freytes DO, Wan LQ, Vunjak-Novakovic G (2009) Geometry and force control of cell function. J Cell Biochem 108(5):1047–1058. https://doi.org/10.1002/jcb.22355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Adams JC, Watt FM (1993) Regulation of development and differentiation by the extracellular matrix. Development (Cambridge, England) 117(4):1183–1198

    Article  CAS  Google Scholar 

  158. Brown RE, Butler JP, Rogers RA, Leith DE (1994) Mechanical connections between elastin and collagen. Connect Tissue Res 30(4):295–308

    Article  CAS  Google Scholar 

  159. Duffy GP, McFadden TM, Byrne EM, Gill SL, Farrell E, O'Brien FJ (2011) Towards in vitro vascularisation of collagen-GAG scaffolds. Eur Cells Mater 21:15–30

    Article  CAS  Google Scholar 

  160. Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R et al (2004) Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A 101(52):18129–18134. https://doi.org/10.1073/pnas.0407817101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Wei HJ, Chen CH, Lee WY, Chiu I, Hwang SM, Lin WW et al (2008) Bioengineered cardiac patch constructed from multilayered mesenchymal stem cells for myocardial repair. Biomaterials. 29(26):3547–3556. https://doi.org/10.1016/j.biomaterials.2008.05.009

    Article  CAS  PubMed  Google Scholar 

  162. Huebsch N, Mooney DJ (2009) Inspiration and application in the evolution of biomaterials. Nature. 462(7272):426–432. https://doi.org/10.1038/nature08601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Williams DF (2009) On the nature of biomaterials. Biomaterials. 30(30):5897–5909. https://doi.org/10.1016/j.biomaterials.2009.07.027

    Article  CAS  PubMed  Google Scholar 

  164. Wainwright JM, Czajka CA, Patel UB, Freytes DO, Tobita K, Gilbert TW et al (2010) Preparation of cardiac extracellular matrix from an intact porcine heart. Tissue Eng C Methods 16(3):525–532. https://doi.org/10.1089/ten.TEC.2009.0392

    Article  CAS  Google Scholar 

  165. Ismagilov RF, Maharbiz MM (2007) Can we build synthetic, multicellular systems by controlling developmental signaling in space and time? Curr Opin Chem Biol 11(6):604–611. https://doi.org/10.1016/j.cbpa.2007.10.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Leor J, Tuvia S, Guetta V, Manczur F, Castel D, Willenz U et al (2009) Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in Swine. J Am Coll Cardiol 54(11):1014–1023. https://doi.org/10.1016/j.jacc.2009.06.010

    Article  PubMed  Google Scholar 

  167. Martens TP, Godier AF, Parks JJ, Wan LQ, Koeckert MS, Eng GM et al (2009) Percutaneous cell delivery into the heart using hydrogels polymerizing in situ. Cell Transplant 18(3):297–304. https://doi.org/10.3727/096368909788534915

    Article  PubMed  Google Scholar 

  168. Rodell CB, Lee ME, Wang H, Takebayashi S, Takayama T, Kawamura T et al (2016) Injectable shear-thinning hydrogels for minimally invasive delivery to infarcted myocardium to limit left ventricular remodeling. Circ Cardiovasc Interv 9(10). https://doi.org/10.1161/circinterventions.116.004058

  169. Johnson TD, Christman KL (2013) Injectable hydrogel therapies and their delivery strategies for treating myocardial infarction. Expert Opin Drug Deliv 10(1):59–72. https://doi.org/10.1517/17425247.2013.739156

    Article  CAS  PubMed  Google Scholar 

  170. Dib N, Campbell A, Jacoby DB, Zawadzka A, Ratliff J, Miedzybrocki BM et al (2006) Safety and feasibility of percutaneous autologous skeletal myoblast transplantation in the coil-infarcted swine myocardium. J Pharmacol Toxicol Methods 54(1):71–77. https://doi.org/10.1016/j.vascn.2005.12.002

    Article  CAS  PubMed  Google Scholar 

  171. Rao SV, Zeymer U, Douglas PS, Al-Khalidi H, Liu J, Gibson CM et al (2015) 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 170(5):929–937. https://doi.org/10.1016/j.ahj.2015.08.017

    Article  CAS  PubMed  Google Scholar 

  172. Rao SV, Zeymer U, Douglas PS, Al-Khalidi H, White JA, Liu J et al (2016) Bioabsorbable intracoronary matrix for prevention of ventricular remodeling after myocardial infarction. J Am Coll Cardiol 68(7):715–723. https://doi.org/10.1016/j.jacc.2016.05.053

    Article  PubMed  Google Scholar 

  173. Mann DL, Lee RJ, Coats AJ, Neagoe G, Dragomir D, Pusineri E et al (2016) 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 18(3):314–325. https://doi.org/10.1002/ejhf.449

    Article  CAS  PubMed  Google Scholar 

  174. Mewhort HE, Turnbull JD, Satriano A, Chow K, Flewitt JA, Andrei AC et al (2016) Epicardial infarct repair with bioinductive extracellular matrix promotes vasculogenesis and myocardial recovery. J Heart Lung Transplant 35(5):661–670. https://doi.org/10.1016/j.healun.2016.01.012

    Article  PubMed  Google Scholar 

  175. Mewhort HE, Turnbull JD, Meijndert HC, Ngu JM, Fedak PW (2014) Epicardial infarct repair with basic fibroblast growth factor-enhanced CorMatrix-ECM biomaterial attenuates postischemic cardiac remodeling. J Thorac Cardiovasc Surg 147(5):1650–1659. https://doi.org/10.1016/j.jtcvs.2013.08.005

    Article  CAS  PubMed  Google Scholar 

  176. Menasche P, Vanneaux V, Hagege A, Bel A, Cholley B, Parouchev A et al (2018) Transplantation of human embryonic stem cell-derived cardiovascular progenitors for severe ischemic left ventricular dysfunction. J Am Coll Cardiol 71(4):429–438. https://doi.org/10.1016/j.jacc.2017.11.047

    Article  PubMed  Google Scholar 

  177. Sahoo S, Losordo DW (2014) Exosomes and cardiac repair after myocardial infarction. Circ Res 114(2):333–344. https://doi.org/10.1161/circresaha.114.300639

    Article  CAS  PubMed  Google Scholar 

  178. Liu B, Lee BW, Nakanishi K, Villasante A, Williamson R, Metz J et al (2018) Cardiac recovery via extended cell-free delivery of extracellular vesicles secreted by cardiomyocytes derived from induced pluripotent stem cells. Nat Biomed Eng 2(5):293–303. https://doi.org/10.1038/s41551-018-0229-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Purcell BP, Lobb D, Charati MB, Dorsey SM, Wade RJ, Zellars KN et al (2014) Injectable and bioresponsive hydrogels for on-demand matrix metalloproteinase inhibition. Nat Mater 13(6):653–661. https://doi.org/10.1038/nmat3922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Wang LL, Liu Y, Chung JJ, Wang T, Gaffey AC, Lu M et al (2017) Local and sustained miRNA delivery from an injectable hydrogel promotes cardiomyocyte proliferation and functional regeneration after ischemic injury. Nat Biomed Eng 1:983–992. https://doi.org/10.1038/s41551-017-0157-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Fan Z, Xu Z, Niu H, Gao N, Guan Y, Li C et al (2018) An injectable oxygen release system to augment cell survival and promote cardiac repair following myocardial infarction. Sci Rep 8(1):1371. https://doi.org/10.1038/s41598-018-19906-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Tang J, Shen D, Caranasos TG, Wang Z, Vandergriff AC, Allen TA et al (2017) Therapeutic microparticles functionalized with biomimetic cardiac stem cell membranes and secretome. Nat Commun 8:13724. https://doi.org/10.1038/ncomms13724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research was funded by Innovation Fund for Medical Sciences (CIFMS, 2016-I2M-1-015); National Natural Science Foundation of China (NSFC, 81770308, 81500239); the National Key Research and Development Project of China (2019YFA0801500); and CAMS Beijing Natural Science Foundation (7172183).

Author information

Authors and Affiliations

  1. State Key Laboratory of Cardiovascular Disease, Fuwai Hospital, National Center for Cardiovascular Disease, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100037, China

    Haotong Li & Yu Nie

  2. Department of Cardiology, Peking University First Hospital, Beijing, China

    Minghui Bao

Authors
  1. Haotong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Minghui Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: Y.N.; Writing: H.L., M.B., and Y.N.; Editing: H.L. and Y.N.

Corresponding author

Correspondence to Yu Nie.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H., Bao, M. & Nie, Y. Extracellular matrix–based biomaterials for cardiac regeneration and repair. Heart Fail Rev 26, 1231–1248 (2021). https://doi.org/10.1007/s10741-020-09953-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10741-020-09953-9

Keywords

Search

Navigation