Skip to main content
SpringerLink
Log in

Biomaterial Interface in Cardiac Cell and Tissue Engineering

  • Chapter
  • First Online:
Advanced Technologies in Cardiovascular Bioengineering

Abstract

Cardiovascular diseases continue to be the leading cause of death while available clinical interventions have limited contributions to heart repair and regeneration. The field of cardiac cell and tissue engineering emerged to provide promising tools for understanding heart remodeling mechanisms and promoting heart repair through the combination of myocardial cells and biomaterials. In this chapter, we introduce the in vitro and in vivo applications of the most recently developed biomaterials, including bulk hydrogels, structural scaffolds and smart materials, for cardiac cell and tissue engineering. The properties of biomaterials and cell-biomaterial interactions could be tuned through various engineering techniques, which play an important role in directing myocardial behaviors, such as differentiation, maturation and phenotypical remodeling. Using these biomaterials, in vitro cardiac models with high physiological relevance have been established and efficient heart regeneration has been verified in many animal models. Although still far from clinical trials due to remained challenges, the “bottom up” design could enable customized assembly of cardiac tissue constructs and increase the merit of cardiac cell and tissue engineering in heart disease treatment.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

2D:

Two dimensional

3D:

Three dimensional

4D:

Four dimensional

ADSCs:

Adipose-derived stem cells

ANG-1:

Angiopoietin-1

BA:

Butyl acrylate

bFGFs:

Basic fibroblast growth factors

CAVD:

Calcific aortic valve disease

CDCs:

Cardiosphere-derived cells

CEST:

Chemical exchange saturation transfer

CHP:

Collagen hybridizing peptide

CMs:

Cardiomyocytes

CNTs:

Carbon nanotubes

CPCs:

Cardiac progenitor cells

DOX:

Doxorubicin

ECM:

Extracellular matrix

ECs:

Endothelial cells

EHTs:

Engineered heart tissues

EPCs:

Endothelial progenitor cells

ESCs:

Embryonic stem cells

hESC-CMs:

Embryonic stem cell derived cardiomyocytes

hESC-MSCs:

Embryonic stem cell derived mesenchymal stem cells

HGF:

Hepatocyte growth factor

hiPSC-CMs:

Human induced pluripotent stem cell derived cardiomyocytes

hiPSCs:

Human induced pluripotent stem cells

IGF-1:

Insulin-like growth factor-1

iPSCs:

Induced pluripotent stem cells

LVEF:

Left ventricular ejection fraction

MCs:

Mural cells

MI:

Myocardial infarction

MMPs:

Matrix metalloproteinases

MRI:

Magnetic resonance imaging

MSCs:

Mesenchymal stem cells

NPs:

Nanoparticles

NRVMs:

Neonatal rat ventricular myocytes

PAN:

Polyacrylonitrile

PCL:

Polycaprolactone

PDMS:

Polydimethylsiloxane

PEG:

Poly(ethylene glycol)

PEGDA:

Poly (ethylene glycol) diacrylate

PF:

Polyethylene glycol-fibrinogen

PGS:

Poly (glycerol sebacate)

PIPAAm:

Poly (N-isopropylacrylamide)

PLGA:

Poly (D,L-lactide-co-glycolide)

PTAA:

Poly (thiophene-3-acetic acid)

PU:

Polyurethane

PVAX:

Peroxalate containing vanillyl alcohol

RGD:

Arginylglycylaspartic acid

RLP:

Resilin-like polypeptide

ROCK:

Rho-associated protein kinase

ROS:

Reactive oxygen species

SMCs:

Smooth muscle cells

SMPs:

Shape memory polymers

SWCNTs:

Single-wall carbon nanotubes

tBA:

tert-butyl acrylate

TNF:

Tumor necrosis factor

tPA:

Tissue plasminogen activator

UPy:

Ureido-pyrimid-inone

VEGFs:

Vascular endothelial growth factors

YAP:

Yes-associated protein

α-CD:

α-cyclodextrin

References

  1. Benjamin, E.J., Blaha, M.J., Chiuve, S.E., Cushman, M., Das, S.R., Deo, R., et al.: Heart disease and stroke statistics-2017 update a report from the American Heart Association. Circulation. 135(10), E146–E603 (2017). https://doi.org/10.1161/Cir.0000000000000485

    Article  Google Scholar 

  2. Laflamme, M.A., Murry, C.E.: Heart regeneration. Nature. 473(7347), 326–335 (2011). https://doi.org/10.1038/nature10147

    Article  Google Scholar 

  3. Hasan, A., Waters, R., Roula, B., Dana, R., Yara, S., Alexandre, T., et al.: Engineered biomaterials to enhance stem cell-based cardiac tissue engineering and therapy. Macromol. Biosci. 16(7), 958–977 (2016). https://doi.org/10.1002/mabi.201500396

    Article  Google Scholar 

  4. Kazbanov, I.V., ten Tusscher, K.H.W.J., Panfilov, A.V.: Effects of heterogeneous diffuse fibrosis on arrhythmia dynamics and mechanism. Sci Rep-Uk. 2016;6. doi: ARTN 20835; https://doi.org/10.1038/srep20835

  5. Ferrario, C.M., Schiffrin, E.L.: Role of mineralocorticoid receptor antagonists in cardiovascular disease. Circ. Res. 116(1), 206–213 (2015). https://doi.org/10.1161/Circresaha.116.302706

    Article  Google Scholar 

  6. Kotecha, D., Holmes, J., Krum, H., Altman, D.G., Manzano, L., Cleland, J.G.F., et al.: Efficacy of beta blockers in patients with heart failure plus atrial fibrillation: an individual-patient data meta-analysis. Lancet. 384(9961), 2235–2243 (2014). https://doi.org/10.1016/S0140-6736(14)61373-8

    Article  Google Scholar 

  7. Sacks, C.A., Jarcho, J.A., Curfman, G.D.: Paradigm shifts in heart-failure therapy – a timeline. New Engl J Med. 371(11), 989–991 (2014). https://doi.org/10.1056/NEJMp1410241

    Article  Google Scholar 

  8. Yacoub, M.: Cardiac donation after circulatory death: a time to reflect. Lancet. 385(9987), 2554–2556 (2015). https://doi.org/10.1016/S0140-6736(15)60683-3

    Article  Google Scholar 

  9. Hirt, M.N., Hansen, A., Eschenhagen, T.: Cardiac tissue engineering state of the art. Circ. Res. 114(2), 354–367 (2014). https://doi.org/10.1161/Circresaha.114.300522

    Article  Google Scholar 

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

    Article  Google Scholar 

  11. Ronaldson-Bouchard, K., Ma, S.P., Yeager, K., Chen, T., Song, L.J., Sirabella, D., et al.: Advanced maturation of human cardiac tissue grown from pluripotent stem cells. Nature. 556(7700), 239 (2018). https://doi.org/10.1038/s41586-018-0016-3

    Article  Google Scholar 

  12. Wang, G., McCain, M.L., Yang, L.H., He, A.B., Pasqualini, F.S., Agarwal, A., et al.: Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat. Med. 20(6), 616–623 (2014). https://doi.org/10.1038/nm.3545

    Article  Google Scholar 

  13. Marsano, A., Conficconi, C., Lemme, M., Occhetta, P., Gaudiello, E., Votta, E., et al.: Beating heart on a chip: a novel microfluidic platform to generate functional 3D cardiac microtissues. Lab Chip. 16(3), 599–610 (2016). https://doi.org/10.1039/c5lc01356a

    Article  Google Scholar 

  14. Soares, C.P., Midlej, V., de Oliveira, M.E.W., Benchimol, M., Costa, M.L., Mermelstein, C.: 2D and 3D-organized cardiac cells shows differences in cellular morphology, adhesion junctions, presence of myofibrils and protein expression. Plos One. 2012;7(5). doi: ARTN e38147; https://doi.org/10.1371/journal.pone.0038147

  15. Nunes, S.S., Miklas, J.W., Liu, J., Aschar-Sobbi, R., Xiao, Y., Zhang, B.Y., et al.: Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat. Methods. 10(8), 781 (2013). https://doi.org/10.1038/Nmeth.2524

    Article  Google Scholar 

  16. Ruan, J.L., Tulloch, N.L., Razumova, M.V., Saiget, M., Muskheli, V., Pabon, L., et al.: Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue. Circulation. 134(20), 1557 (2016). https://doi.org/10.1161/Circulationaha.114.014998

    Article  Google Scholar 

  17. Hinson, J.T., Chopra, A., Nafissi, N., Polacheck, W.J., Benson, C.C., Swist, S., et al.: Titin mutations in iPS cells define sarcomere insufficiency as a cause of dilated cardiomyopathy. Science. 349(6251), 982–986 (2015). https://doi.org/10.1126/science.aaa5458

    Article  Google Scholar 

  18. Ma, Z., Huebsch, N., Koo, S., Mandegar, M.A., Siemons, B., Boggess, S., et al.: Contractile deficits in engineered cardiac microtissues as a result of MYBPC3 deficiency and mechanical overload. Nat Biomed Eng. 2(12), 955–967 (2018). https://doi.org/10.1038/s41551-018-0280-4

    Article  Google Scholar 

  19. Malan, D., Zhang, M., Stallmeyer, B., Muller, J., Fleischmann, B.K., Schulze-Bahr, E., et al.: Human iPS cell model of type 3 long QT syndrome recapitulates drug-based phenotype correction. Basic Res Cardiol. 2016;111(2). doi: ARTN 14; https://doi.org/10.1007/s00395-016-0530-0

  20. Shinozawa, T., Nakamura, K., Shoji, M., Morita, M., Kimura, M., Furukawa, H., et al.: Recapitulation of clinical individual susceptibility to drug-induced QT prolongation in healthy subjects using iPSC-derived cardiomyocytes. Stem Cell Rep. 8(2), 226–234 (2017). https://doi.org/10.1016/j.stemcr.2016.12.014

    Article  Google Scholar 

  21. Zhang, Y.S., Yue, K., Aleman, J., Moghaddam, K.M., Bakht, S.M., Yang, J., et al.: 3D bioprinting for tissue and organ fabrication. Ann. Biomed. Eng. 45(1), 148–163 (2017). https://doi.org/10.1007/s10439-016-1612-8

    Article  Google Scholar 

  22. Hashimoto, H., Olson, E.N., Bassel-Duby, R.: Therapeutic approaches for cardiac regeneration and repair. Nat. Rev. Cardiol. 15(10), 585–600 (2018). https://doi.org/10.1038/s41569-018-0036-6

    Article  Google Scholar 

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

    Article  Google Scholar 

  24. Volarevic, V., Markovic, B.S., Gazdic, M., Volarevic, A., Jovicic, N., Arsenijevic, N., et al.: Ethical and safety issues of stem cell-based therapy. Int. J. Med. Sci. 15(1), 36–45 (2018). https://doi.org/10.7150/ijms.21666

    Article  Google Scholar 

  25. Roche, E.T., Hastings, C.L., Lewin, S.A., Shvartsman, D.E., Brudno, Y., Vasilyev, N.V., et al.: Comparison of biomaterial delivery vehicles for improving acute retention of stem cells in the infarcted heart. Biomaterials. 35(25), 6850–6858 (2014). https://doi.org/10.1016/j.biomaterials.2014.04.114

    Article  Google Scholar 

  26. Lee, E.J., Kasper, F.K., Mikos, A.G.: Biomaterials for tissue engineering. Ann. Biomed. Eng. 42(2), 323–337 (2014). https://doi.org/10.1007/s10439-013-0859-6

    Article  Google Scholar 

  27. McCain, M.L., Agarwal, A., Nesmith, H.W., Nesmith, A.P., Parker, K.K.: Micromolded gelatin hydrogels for extended culture of engineered cardiac tissues. Biomaterials. 35(21), 5462–5471 (2014). https://doi.org/10.1016/j.biomaterials.2014.03.052

    Article  Google Scholar 

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

    Article  Google Scholar 

  29. Williams, C., Budina, E., Stoppel, W.L., Sullivan, K.E., Emani, S., Emani, S.M., et al.: Cardiac extracellular matrix-fibrin hybrid scaffolds with tunable properties for cardiovascular tissue engineering. Acta Biomater. 14, 84–95 (2015). https://doi.org/10.1016/j.actbio.2014.11.035

    Article  Google Scholar 

  30. Aghdam, R.M., Shakhesi, S., Najarian, S., Mohammadi, M.M., Tafti, S.H.A., Mirzadeh, H.: Fabrication of a nanofibrous scaffold for the in vitro culture of cardiac progenitor cells for myocardial regeneration. Int J Polym Mater Po. 63(5), 229–239 (2014). https://doi.org/10.1080/00914037.2013.800983

    Article  Google Scholar 

  31. Chiono, V., Mozetic, P., Boffito, M., Sartori, S., Gioffredi, E., Silvestri, A., et al.: Polyurethane-based scaffolds for myocardial tissue engineering. Interface Focus. 2014;4(1). doi: ARTN 20130045; https://doi.org/10.1098/rsfs.2013.0045

  32. Flaig, F., Ragot, H., Simon, A., Revet, G., Kitsara, M., Kitasato, L., et al.: Design of functional electrospun scaffolds based on poly(glycerol sebacate) elastomer and poly(lactic acid) for cardiac tissue engineering. ACS Biomater Sci. Eng. 6(4), 2388–2400 (2020). https://doi.org/10.1021/acsbiomaterials.0c00243

    Article  Google Scholar 

  33. Crowder, S.W., Liang, Y., Rath, R., Park, A.M., Maltais, S., Pintauro, P.N., et al.: Poly(epsilon-caprolactone)-carbon nanotube composite scaffolds for enhanced cardiac differentiation of human mesenchymal stem cells. Nanomedicine-Uk. 8(11), 1763–1776 (2013). https://doi.org/10.2217/nnm.12.204

    Article  Google Scholar 

  34. Karakikes, I., Ameen, M., Termglinchan, V., Wu, J.C.: Human induced pluripotent stem cell-derived cardiomyocytes insights into molecular, cellular, and functional phenotypes. Circ. Res. 117(1), 80–88 (2015). https://doi.org/10.1161/Circresaha.117.305365

    Article  Google Scholar 

  35. Prabhakaran, M.P., Mobarakeh, L.G., Kai, D., Karbalaie, K., Nasr-Esfahani, M.H., Ramakrishna, S.: Differentiation of embryonic stem cells to cardiomyocytes on electrospun nanofibrous substrates. J Biomed Mater Res B. 102(3), 447–454 (2014). https://doi.org/10.1002/jbm.b.33022

    Article  Google Scholar 

  36. Chen, I.Y., Matsa, E., Wu, J.C.: Induced pluripotent stem cells: at the heart of cardiovascular precision medicine. Nat. Rev. Cardiol. 13(6), 333–349 (2016). https://doi.org/10.1038/nrcardio.2016.36

    Article  Google Scholar 

  37. Mandegar, M.A., Huebsch, N., Frolov, E.B., Shin, E., Truong, A., Olvera, M.P., et al.: CRISPR interference efficiently induces specific and reversible gene silencing in human iPSCs. Cell Stem Cell. 18(4), 541–553 (2016). https://doi.org/10.1016/j.stem.2016.01.022

    Article  Google Scholar 

  38. Hatoum, H., Dasi, L.P.: Reduction of pressure gradient and turbulence using vortex generators in prosthetic heart valves. Ann. Biomed. Eng. 47(1), 85–96 (2019). https://doi.org/10.1007/s10439-018-02128-6

    Article  Google Scholar 

  39. Lu, L., Mende, M., Yang, X.G., Korber, H.F., Schnittler, H.J., Weinert, S., et al.: Design and validation of a bioreactor for simulating the cardiac niche: a system incorporating cyclic stretch, electrical stimulation, and constant perfusion. Tissue Eng Pt A. 19(3–4), 403–414 (2013). https://doi.org/10.1089/ten.tea.2012.0135

    Article  Google Scholar 

  40. Paez-Mayorga, J., Hernandez-Vargas, G., Ruiz-Esparza, G.U., Iqbal, H.M.N., Wang, X.C., Zhang, Y.S., et al.: Bioreactors for cardiac tissue engineering. Adv Healthc Mater. 2019;8(7). doi: ARTN 1701504; 10.1002/adhm.201701504

    Google Scholar 

  41. Zhu, J.M., Marchant, R.E.: Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Devic. 8(5), 607–626 (2011). https://doi.org/10.1586/Erd.11.27

    Article  Google Scholar 

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

    Article  Google Scholar 

  43. Vedadghavami, A., Minooei, F., Mohammadi, M.H., Khetani, S., Kolahchi, A.R., Mashayekhan, S., et al.: Manufacturing of hydrogel biomaterials with controlled mechanical properties for tissue engineering applications. Acta Biomater. 62, 42–63 (2017). https://doi.org/10.1016/j.actbio.2017.07.028

    Article  Google Scholar 

  44. Goldfracht, I., Efraim, Y., Shinnawi, R., Kovalev, E., Huber, I., Gepstein, A., et al.: Engineered heart tissue models from hiPSC-derived cardiomyocytes and cardiac ECM for disease modeling and drug testing applications. Acta Biomater. 92, 145–159 (2019). https://doi.org/10.1016/j.actbio.2019.05.016

    Article  Google Scholar 

  45. Puperi, D.S., Balaoing, L.R., O’Connell, R.W., West, J.L., Grande-Allen, K.J.: 3-dimensional spatially organized PEG-based hydrogels for an aortic valve co-culture model. Biomaterials. 67, 354–364 (2015). https://doi.org/10.1016/j.biomaterials.2015.07.039

    Article  Google Scholar 

  46. Shah, M., Pawan, K.C., Zhang, G.: In vivo assessment of decellularized porcine myocardial slice as an acellular cardiac patch. ACS Appl. Mater. Interfaces. 11(27), 23893–23900 (2019). https://doi.org/10.1021/acsami.9b06453

    Article  Google Scholar 

  47. Boopathy, A.V., Che, P.L., Somasuntharam, I., Fiore, V.F., Cabigas, E.B., Ban, K., et al.: The modulation of cardiac progenitor cell function by hydrogel-dependent Notch1 activation. Biomaterials. 35(28), 8103–8112 (2014). https://doi.org/10.1016/j.biomaterials.2014.05.082

    Article  Google Scholar 

  48. Das, S., Kim, S.W., Choi, Y.J., Lee, S., Lee, S.H., Kong, J.S., et al.: Decellularized extracellular matrix bioinks and the external stimuli to enhance cardiac tissue development in vitro. Acta Biomater. 95, 188–200 (2019). https://doi.org/10.1016/j.actbio.2019.04.026

    Article  Google Scholar 

  49. Zhang, W., Kong, C.W., Tong, M.H., Chooi, W.H., Huang, N., Li, R.A., et al.: Maturation of human embryonic stem cell-derived cardiomyocytes (hESC-CMs) in 3D collagen matrix: effects of niche cell supplementation and mechanical stimulation. Acta Biomater. 49, 204–217 (2017). https://doi.org/10.1016/j.actbio.2016.11.058

    Article  Google Scholar 

  50. Hirt, M.N., Werner, T., Indenbirken, D., Alawi, M., Demin, P., Kunze, A.C., et al.: Deciphering the microRNA signature of pathological cardiac hypertrophy by engineered heart tissue- and sequencing-technology. J. Mol. Cell. Cardiol. 81, 1–9 (2015). https://doi.org/10.1016/j.yjmcc.2015.01.008

    Article  Google Scholar 

  51. Agarwal, A., Farouz, Y., Nesmith, A.P., Deravi, L.F., McCain, M.L., Parker, K.K.: Micropatterning alginate substrates for in vitro cardiovascular muscle on a chip. Adv. Funct. Mater. 23(30), 3738–3746 (2013)

    Article  Google Scholar 

  52. Zhang, X., Xu, B., Puperi, D.S., Yonezawa, A.L., Wu, Y., Tseng, H., et al.: Integrating valve-inspired design features into poly(ethylene glycol) hydrogel scaffolds for heart valve tissue engineering. Acta Biomater. 14, 11–21 (2015). https://doi.org/10.1016/j.actbio.2014.11.042

    Article  Google Scholar 

  53. Zhao, H., Li, X.K., Zhao, S., Zeng, Y., Zhao, L., Ding, H.Y., et al.: Microengineered in vitro model of cardiac fibrosis through modulating myofibroblast mechanotransduction. Biofabrication. 2014;6(4). doi: Artn 045009; https://doi.org/10.1088/1758-5082/6/4/045009

  54. Grant, R., Hay, D.C., Callanan, A.: A drug-induced hybrid electrospun poly-capro-lactone: cell-derived extracellular matrix scaffold for liver tissue engineering. Tissue Eng Pt A. 23(13–14), 650–662 (2017). https://doi.org/10.1089/ten.tea.2016.0419

    Article  Google Scholar 

  55. Grover, G.N., Rao, N., Christman, K.L.: Myocardial matrix-polyethylene glycol hybrid hydrogels for tissue engineering. Nanotechnology. 2014;25(1). doi: Artn 014011; https://doi.org/10.1088/0957-4484/25/1/014011

  56. Kumar, A., Rao, K.M., Han, S.S.: Synthesis of mechanically stiff and bioactive hybrid hydrogels for bone tissue engineering applications. Chem. Eng. J. 317, 119–131 (2017). https://doi.org/10.1016/j.cej.2017.02.065

    Article  Google Scholar 

  57. Duan, B., Yin, Z.Y., Kang, L.H., Magin, R.L., Butcher, J.T.: Active tissue stiffness modulation controls valve interstitial cell phenotype and osteogenic potential in 3D culture. Acta Biomater. 36, 42–54 (2016). https://doi.org/10.1016/j.actbio.2016.03.007

    Article  Google Scholar 

  58. McGann, C.L., Levenson, E.A., Kiick, K.L.: Resilin-based hybrid hydrogels for cardiovascular tissue engineering. Macromol. Chem. Phys. 214(2), 203–213 (2013). https://doi.org/10.1002/macp.201200412

    Article  Google Scholar 

  59. Yang, B.G., Yao, F.L., Hao, T., Fang, W.C., Ye, L., Zhang, Y.B., et al.: Development of electrically conductive double-network hydrogels via one-step facile strategy for cardiac tissue engineering. Adv. Healthc. Mater. 5(4), 474–488 (2016). https://doi.org/10.1002/adhm.201500520

    Article  Google Scholar 

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

    Article  Google Scholar 

  61. Radhakrishnan, J., Krishnan, U.M., Sethuraman, S.: Hydrogel based injectable scaffolds for cardiac tissue regeneration. Biotechnol. Adv. 32(2), 449–461 (2014). https://doi.org/10.1016/j.biotechadv.2013.12.010

    Article  Google Scholar 

  62. Sabbah, H.N., Wang, M.J., Gupta, R.C., Rastogi, S., Ilsar, I., Sabbah, M.S., et al.: 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. 1(3), 252–258 (2013). https://doi.org/10.1016/j.jchf.2013.02.006

    Article  Google Scholar 

  63. Waters, R., Alam, P., Pacelli, S., Chakravarti, A.R., Ahmed, R.P.H., Paul, A.: Stem cell-inspired secretome-rich injectable hydrogel to repair injured cardiac tissue. Acta Biomater. 69, 95–106 (2018). https://doi.org/10.1016/j.actbio.2017.12.025

    Article  Google Scholar 

  64. Levit, R.D., Landazuri, N., Phelps, E.A., Brown, M.E., Garcia, A.J., Davis, M.E., et al.: Cellular encapsulation enhances cardiac repair. J Am Heart Assoc. 2013;2(5). doi: ARTN e000367; https://doi.org/10.1161/JAHA.113.000367

  65. Tran, C., Damaser, M.S.: Stem cells as drug delivery methods: Application of stem cell secretome for regeneration. Adv Drug Deliver Rev. 2015;82–83:1–11. https://doi.org/10.1016/j.addr.2014.10.007

  66. Hasan, A., Khattab, A., Islam, M.A., Abou Hweij, K., Zeitouny, J., Waters, R., et al.: Injectable hydrogels for cardiac tissue repair after myocardial infarction. Adv Sci. 2015;2(11). doi: ARTN 1500122; 10.1002/advs.201500122

    Google Scholar 

  67. Rufaihah, A.J., Johari, N.A., Vaibavi, S.R., Plotkin, M., Thien, D.T.D., Kofidis, T., et al.: Dual delivery of VEGF and ANG-1 in ischemic hearts using an injectable hydrogel. Acta Biomater. 48, 58–67 (2017). https://doi.org/10.1016/j.actbio.2016.10.013

    Article  Google Scholar 

  68. Paul, A., Hasan, A., Al Kindi, H., Gaharwar, A.K., Rao, V.T.S., Nikkhah, M., et al.: Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair. ACS Nano. 8(8), 8050–8062 (2014). https://doi.org/10.1021/nn5020787

    Article  Google Scholar 

  69. Mihalko, E., Huang, K., Sproul, E., Cheng, K., Brown, A.C.: Targeted treatment of lschemic and fibrotic complications of myocardial infarction using a dual-delivery microgel therapeutic. ACS Nano. 12(8), 7826–7837 (2018). https://doi.org/10.1021/acsnano.8b01977

    Article  Google Scholar 

  70. Rajabi-Zeleti, S., Jalili-Firoozinezhad, S., Azarnia, M., Khayyatan, F., Vandat, S., Nikeghbalian, S., et al.: The behavior of cardiac progenitor cells on macroporous pericardium-derived scaffolds. Biomaterials. 35(3), 970–982 (2014). https://doi.org/10.1016/j.biomaterials.2013.10.045

    Article  Google Scholar 

  71. Fan CX, Shi JJ, Zhuang Y, Zhang LL, Huang L, Yang W, et al. Myocardial-infarction-responsive smart hydrogels targeting matrix metalloproteinase for on-demand growth factor delivery. Adv Mater. 2019;31(40). doi: ARTN 1902900; https://doi.org/10.1002/adma.201902900

  72. MacQueen, L.A., Sheehy, S.P., Chantre, C.O., Zimmerman, J.F., Pasqualini, F.S., Liu, X.J., et al.: A tissue-engineered scale model of the heart ventricle. Nat Biomed Eng. 2(12), 930–941 (2018). https://doi.org/10.1038/s41551-018-0271-5

    Article  Google Scholar 

  73. Liu, W., Zhong, Z., Hu, N., Zhou, Y., Maggio, L., Miri, A., et al.: Coaxial extrusion bioprinting of 3D microfibrous constructs with cell-favorable gelatin methacryloyl microenvironments. Biofabrication. (2017). https://doi.org/10.1088/1758-5090/aa9d44

  74. Hollister, S.J.: Porous scaffold design for tissue engineering. Nat. Mater. 4(7), 518–524 (2005). https://doi.org/10.1038/nmat1421

    Article  Google Scholar 

  75. Loh, Q.L., Choong, C.: Three-dimensional scaffolds for tissue engineering applications: role of porosity and pore size. Tissue Eng Part B-Re. 19(6), 485–502 (2013). https://doi.org/10.1089/ten.teb.2012.0437

    Article  Google Scholar 

  76. Ambekar, R.S., Kandasubramanian, B.: Progress in the advancement of porous biopolymer scaffold: tissue engineering application. Ind. Eng. Chem. Res. 58(16), 6163–6194 (2019). https://doi.org/10.1021/acs.iecr.8b05334

    Article  Google Scholar 

  77. Pok, S., Myers, J.D., Madihally, S.V., Jacot, J.G.: A multilayered scaffold of a chitosan and gelatin hydrogel supported by a PCL core for cardiac tissue engineering. Acta Biomater. 9(3), 5630–5642 (2013). https://doi.org/10.1016/j.actbio.2012.10.032

    Article  Google Scholar 

  78. Wang, Y.Y., Hu, J., Jiao, J., Liu, Z.N., Zhou, Z., Zhao, C., et al.: Engineering vascular tissue with functional smooth muscle cells derived from human iPS cells and nanofibrous scaffolds. Biomaterials. 35(32), 8960–8969 (2014). https://doi.org/10.1016/j.biomaterials.2014.07.011

    Article  Google Scholar 

  79. Bian, W.N., Jackman, C.P., Bursac, N.: Controlling the structural and functional anisotropy of engineered cardiac tissues. Biofabrication. 2014;6(2). doi: Artn 024109; 10.1088/1758-5082/6/2/024109

    Google Scholar 

  80. Engelmayr, G.C., Cheng, M.Y., Bettinger, C.J., Borenstein, J.T., Langer, R., Freed, L.E.: Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat. Mater. 7(12), 1003–1010 (2008). https://doi.org/10.1038/nmat2316

    Article  Google Scholar 

  81. Zieber, L., Or, S., Ruvinov, E., Cohen, S.: Microfabrication of channel arrays promotes vessel-like network formation in cardiac cell construct and vascularization in vivo. Biofabrication. 2014;6(2). doi: Artn 024102; 10.1088/1758-5082/6/2/024102

    Google Scholar 

  82. Fang, Y.C., Zhang, T., Zhang, L., Gong, W.F., Sun, W.: Biomimetic design and fabrication of scaffolds integrating oriented micro-pores with branched channel networks for myocardial tissue engineering. Biofabrication. 2019;11(3). doi: ARTN 035004; 10.1088/1758-5090/ab0fd3

    Google Scholar 

  83. Madden, L.R., Mortisen, D.J., Sussman, E.M., Dupras, S.K., Fugate, J.A., Cuy, J.L., et al.: Proangiogenic scaffolds as functional templates for cardiac tissue engineering. P Natl Acad Sci USA. 107(34), 15211–15216 (2010). https://doi.org/10.1073/pnas.1006442107

    Article  Google Scholar 

  84. Miyagi, Y., Chiu, L.L.Y., Cimini, M., Weisel, R.D., Radisic, M., Li, R.K.: Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. Biomaterials. 32(5), 1280–1290 (2011). https://doi.org/10.1016/j.biomaterials.2010.10.007

    Article  Google Scholar 

  85. Jun, I., Han, H.S., Edwards, J.R., Jeon, H.: Electrospun fibrous scaffolds for tissue engineering: viewpoints on architecture and fabrication. Int J Mol Sci. 2018;19(3). Doi: ARTN 745; 10.3390/ijms19030745

    Google Scholar 

  86. Capulli, A.K., MacQueen, L.A., Sheehy, S.P., Parker, K.K.: Fibrous scaffolds for building hearts and heart parts. Adv Drug Deliver Rev. 96, 83–102 (2016). https://doi.org/10.1016/j.addr.2015.11.020

    Article  Google Scholar 

  87. Ma, Z., Koo, S., Finnegan, M.A., Loskill, P., Huebsch, N., Marks, N.C., et al.: Three-dimensional filamentous human diseased cardiac tissue model. Biomaterials. 35(5), 1367–1377 (2014). https://doi.org/10.1016/j.biomaterials.2013.10.052

    Article  Google Scholar 

  88. Zhang, Y.S., Arneri, A., Bersini, S., Shin, S.R., Zhu, K., Goli-Malekabadi, Z., et al.: Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials. 110, 45–59 (2016). https://doi.org/10.1016/j.biomaterials.2016.09.003

    Article  Google Scholar 

  89. Parrag, I.C., Zandstra, P.W., Woodhouse, K.A.: Fiber alignment and coculture with fibroblasts improves the differentiated phenotype of murine embryonic stem cell-derived cardiomyocytes for cardiac tissue engineering. Biotechnol. Bioeng. 109(3), 813–822 (2012). https://doi.org/10.1002/bit.23353

    Article  Google Scholar 

  90. Kharaziha, M., Nikkhah, M., Shin, S.R., Annabi, N., Masoumi, N., Gaharwar, A.K., et al.: PGS:Gelatin nanofibrous scaffolds with tunable mechanical and structural properties for engineering cardiac tissues. Biomaterials. 34(27), 6355–6366 (2013). https://doi.org/10.1016/j.biomaterials.2013.04.045

    Article  Google Scholar 

  91. Wu, S., Duan, B., Qin, X.H., Butcher, J.T.: Living nano-micro fibrous woven fabric/hydrogel composite scaffolds for heart valve engineering. Acta Biomater. 51, 89–100 (2017). https://doi.org/10.1016/j.actbio.2017.01.051

    Article  Google Scholar 

  92. Fleischer, S., Feiner, R., Shapira, A., Ji, J., Sui, X.M., Wagner, H.D., et al.: Spring-like fibers for cardiac tissue engineering. Biomaterials. 34(34), 8599–8606 (2013). https://doi.org/10.1016/j.biomaterials.2013.07.054

    Article  Google Scholar 

  93. Zhao, G.X., Zhang, X.H., Lu, T.J., Xu, F.: Recent advances in electrospun Nanofibrous scaffolds for cardiac tissue engineering. Adv. Funct. Mater. 25(36), 5726–5738 (2015). https://doi.org/10.1002/adfm.201502142

    Article  Google Scholar 

  94. Ravichandran, R., Venugopal, J.R., Mukherjee, S., Sundarrajan, S., Ramakrishna, S.: Elastomeric core/shell nanofibrous cardiac patch as a biomimetic support for infarcted porcine myocardium. Tissue Eng Pt A. 21(7–8), 1288–1298 (2015). https://doi.org/10.1089/ten.tea.2014.0265

    Article  Google Scholar 

  95. Wang, C., Koo, S., Park, M., Vangelatos, Z., Hoang, P., Conklin, B.R., et al.: Maladaptive contractility of 3D human cardiac microtissues to mechanical nonuniformity. Adv. Healthc. Mater. 9(8), e1901373 (2020)

    Article  Google Scholar 

  96. Badeau, B.A., DeForest, C.A.: Programming stimuli-responsive behavior into biomaterials. Annu. Rev. Biomed. Eng. 21, 241–265 (2019). https://doi.org/10.1146/annurev-bioeng-060418-052324

    Article  Google Scholar 

  97. Uto, K., Tsui, J.H., DeForest, C.A., Kim, D.H.: Dynamically tunable cell culture platforms for tissue engineering and mechanobiology. Prog. Polym. Sci. 65, 53–82 (2017). https://doi.org/10.1016/j.progpolymsci.2016.09.004

    Article  Google Scholar 

  98. Chaudhuri, O., Gu, L., Klumpers, D., Darnell, M., Bencherif, S.A., Weaver, J.C., et al.: Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat. Mater. 15(3), 326 (2016). https://doi.org/10.1038/Nmat4489

    Article  Google Scholar 

  99. Yang, H., Wang, Q., Huang, S., Xiao, A., Li, F.Y., Gan, L., et al.: Smart pH/redox dual-responsive nanogels for on-demand intracellular anticancer drug release. ACS Appl. Mater. Interfaces. 8(12), 7729–7738 (2016). https://doi.org/10.1021/acsami.6b01602

    Article  Google Scholar 

  100. Sponchioni, M., Palmiero, U.C., Moscatelli, D.: Thermo-responsive polymers: applications of smart materials in drug delivery and tissue engineering. Mat Sci Eng C-Mater. 102, 589–605 (2019). https://doi.org/10.1016/j.msec.2019.04.069

    Article  Google Scholar 

  101. Shimizu, T., Yamoto, M., Kikuchi, A., Okano, T.: Two-dimensional manipulation of cardiac myocyte sheets utilizing temperature-responsive culture dishes augments the pulsatile amplitude. Tissue Eng. 7(2), 141–151 (2001). https://doi.org/10.1089/107632701300062732

    Article  Google Scholar 

  102. Sung, T.C., Su, H.C., Ling, Q.D., Kumar, S.S., Chang, Y., Hsu, S.T., et al.: Efficient differentiation of human pluripotent stem cells into cardiomyocytes on cell sorting thermoresponsive surface. Biomaterials. 2020;253. doi: ARTN 120060; 10.1016/j.biomaterials.2020.120060

    Google Scholar 

  103. Sun, S., Shi, H., Moore, S., Wang, C., Ash-Shakoor, A., Mather, P.T., et al.: Progressive myofibril reorganization of human cardiomyocytes on a dynamic nanotopographic substrate. ACS Appl. Mater. Interfaces. 12(19), 21450–21462 (2020)

    Article  Google Scholar 

  104. Vong, L.B., Bui, T.Q., Tomita, T., Sakamoto, H., Hiramatsu, Y., Nagasaki, Y.: Novel angiogenesis therapeutics by redox injectable hydrogel – regulation of local nitric oxide generation for effective cardiovascular therapy. Biomaterials. 167, 143–152 (2018). https://doi.org/10.1016/j.biomaterials.2018.03.023

    Article  Google Scholar 

  105. Masumoto, H., Matsuo, T., Yamamizu, K., Uosaki, H., Narazaki, G., Katayama, S., et al.: Pluripotent stem cell-engineered cell sheets reassembled with defined cardiovascular populations ameliorate reduction in infarct heart function through cardiomyocyte-mediated neovascularization. Stem Cells. 30(6), 1196–1205 (2012). https://doi.org/10.1002/stem.1089

    Article  Google Scholar 

  106. Young, J.L., Engler, A.J.: Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro. Biomaterials. 32(4), 1002–1009 (2011). https://doi.org/10.1016/j.biomaterials.2010.10.020

    Article  Google Scholar 

  107. Corbin, E.A., Vite, A., Peyster, E.G., Bhoovalam, M., Brandimarto, J., Wang, X., et al.: Tunable and reversible substrate stiffness reveals a dynamic mechanosensitivity of cardiomyocytes. ACS Appl. Mater. Interfaces. 11(23), 20603–20614 (2019). https://doi.org/10.1021/acsami.9b02446

    Article  Google Scholar 

  108. Leng, J.S., Lan, X., Liu, Y.J., Du, S.Y.: Shape-memory polymers and their composites: stimulus methods and applications. Prog. Mater. Sci. 56(7), 1077–1135 (2011). https://doi.org/10.1016/j.pmatsci.2011.03.001

    Article  Google Scholar 

  109. Le, D.M., Kulangara, K., Adler, A.F., Leong, K.W., Ashby, V.S.: Dynamic topographical control of mesenchymal stem cells by culture on responsive poly(epsilon-caprolactone) surfaces. Adv. Mater. 23(29), 3278 (2011). https://doi.org/10.1002/adma.201100821

    Article  Google Scholar 

  110. Mengsteab, P.Y., Uto, K., Smith, A.S.T., Frankel, S., Fisher, E., Nawas, Z., et al.: Spatiotemporal control of cardiac anisotropy using dynamic nanotopographic cues. Biomaterials. 86, 1–10 (2016). https://doi.org/10.1016/j.biomaterials.2016.01.062

    Article  Google Scholar 

  111. Bastings, M.M.C., Koudstaal, S., Kieltyka, R.E., Nakano, Y., Pape, A.C.H., Feyen, D.A.M., et al.: A fast pH-switchable and self-healing supramolecular hydrogel carrier for guided, local catheter injection in the infarcted myocardium. Adv. Healthc. Mater. 3(1), 70–78 (2014). https://doi.org/10.1002/adhm.201300076

    Article  Google Scholar 

  112. Wang, Q., Mynar, J.L., Yoshida, M., Lee, E., Lee, M., Okuro, K., et al.: High-water-content mouldable hydrogels by mixing clay and a dendritic molecular binder. Nature. 463(7279), 339–343 (2010). https://doi.org/10.1038/nature08693

    Article  Google Scholar 

  113. Yang, Y.H., Liu, C.H., Liang, Y.H., Lin, F.H., Wu, K.C.W.: Hollow mesoporous hydroxyapatite nanoparticles (hmHANPs) with enhanced drug loading and pH-responsive release properties for intracellular drug delivery. J. Mater. Chem. B. 1(19), 2447–2450 (2013). https://doi.org/10.1039/c3tb20365d

    Article  Google Scholar 

  114. Kreyling, W.G., Abdelmonem, A.M., Ali, Z., Alves, F., Geiser, M., Haberl, N., et al.: In vivo integrity of polymer-coated gold nanoparticles. Nat. Nanotechnol. 10(7), 619 (2015). https://doi.org/10.1038/Nnano.2015.111

    Article  Google Scholar 

  115. Li, X., Zhou, J., Liu, Z.Q., Chen, J., Lu, S.H., Sun, H.Y., et al.: A PNIPAAm-based thermosensitive hydrogel containing SWCNTs for stem cell transplantation in myocardial repair. Biomaterials. 35(22), 5679–5688 (2014). https://doi.org/10.1016/j.biomaterials.2014.03.067

    Article  Google Scholar 

  116. Li, Z.Q., Fan, Z.B., Xu, Y.Y., Lo, W.S., Wang, X., Niu, H., et al.: pH-sensitive and thermosensitive hydrogels as stem-cell carriers for cardiac therapy. ACS Appl. Mater. Interfaces. 8(17), 10752–10760 (2016). https://doi.org/10.1021/acsami.6b01374

    Article  Google Scholar 

  117. Yabluchanskiy, A., Ma, Y.G., Iyer, R.P., Hall, M.E., Lindsey, M.L.: Matrix metalloproteinase-9: many shades of function in cardiovascular disease. Physiology. 28(6), 391–403 (2013). https://doi.org/10.1152/physiol.00029.2013

    Article  Google Scholar 

  118. Nguyen, M.M., Carlini, A.S., Chien, M.P., Sonnenberg, S., Luo, C.L., Braden, R.L., et al.: Enzyme-responsive nanoparticles for targeted accumulation and prolonged retention in heart tissue after myocardial infarction. Adv. Mater. 27(37), 5547–5552 (2015). https://doi.org/10.1002/adma.201502003

    Article  Google Scholar 

  119. Hao, T., Li, J.J., Yao, F.L., Dong, D.Y., Wang, Y., Yang, B.G., et al.: Injectable fullerenol/alginate hydrogel for suppression of oxidative stress damage in Brown adipose-derived stem cells and cardiac repair. ACS Nano. 11(6), 5474–5488 (2017). https://doi.org/10.1021/acsnano.7b00221

    Article  Google Scholar 

  120. Park, S., Yoon, J., Bae, S., Park, M., Kang, C., Ke, Q.G., et al.: Therapeutic use of H2O2-responsive anti-oxidant polymer nanoparticles for doxorubicin-induced cardiomyopathy. Biomaterials. 35(22), 5944–5953 (2014). https://doi.org/10.1016/j.biomaterials.2014.03.084

    Article  Google Scholar 

  121. Tan, S.Y., Teh, C., Ang, C.Y., Li, M.H., Li, P.Z., Korzh, V., et al.: Responsive mesoporous silica nanoparticles for sensing of hydrogen peroxide and simultaneous treatment toward heart failure. Nanoscale. 9(6), 2253–2261 (2017). https://doi.org/10.1039/c6nr08869d

    Article  Google Scholar 

  122. Lee, J., Manoharan, V., Cheung, L., Lee, S., Cha, B.H., Newman, P., et al.: Nanoparticle-based hybrid scaffolds for deciphering the role of multimodal cues in cardiac tissue engineering. ACS Nano. 13(11), 12525–12539 (2019). https://doi.org/10.1021/acsnano.9b03050

    Article  Google Scholar 

  123. Holzl K, Lin SM, Tytgat L, Van Vlierberghe S, Gu LX, Ovsianikov A. Bioink properties before, during and after 3D bioprinting. Biofabrication. 2016;8(3). doi: Artn 032002; 10.1088/1758-5090/8/3/032002

    Google Scholar 

  124. Zhao, Y., Rafatian, N., Feric, N.T., Cox, B.J., Aschar-Sobbi, R., Wang, E.Y., et al.: A platform for generation of chamber-specific cardiac tissues and disease Modeling. Cell. 176(4), 913 (2019). https://doi.org/10.1016/j.cell.2018.11.042

    Article  Google Scholar 

  125. Montag, J., Petersen, B., Flogel, A.K., Becker, E., Lucas-Hahn, A., Cost, G.J., et al.: Successful knock-in of hypertrophic cardiomyopathy-mutation R723G into the MYH7 gene mimics HCM pathology in pigs. Sci Rep-Uk. 2018;8. doi: ARTN 4786; 10.1038/s41598-018-22936-z

    Google Scholar 

  126. Paunovska, K., Sago, C.D., Monaco, C.M., Hudson, W.H., Castro, M.G., Rudoltz, T.G., et al.: A direct comparison of in vitro and in vivo nucleic acid delivery mediated by hundreds of nanoparticles reveals a weak correlation. Nano Lett. 18(3), 2148–2157 (2018). https://doi.org/10.1021/acs.nanolett.8b00432

    Article  Google Scholar 

  127. Hwang, J., Huang, Y.F., Burwell, T.J., Peterson, N.C., Connor, J., Weiss, S.J., et al.: In situ imaging of tissue remodeling with collagen hybridizing peptides. ACS Nano. 11(10), 9825–9835 (2017). https://doi.org/10.1021/acsnano.7b03150

    Article  Google Scholar 

  128. Ouyang, L.L., Armstrong, J.P.K., Salmeron-Sanchez, M., Stevens, M.M.: Assembling living building blocks to engineer complex tissues. Adv Funct Mater. 2020;30(26). doi: ARTN 1909009; https://doi.org/10.1002/adfm.201909009

  129. Fleischer, S., Shapira, A., Feiner, R., Dvir, T.: Modular assembly of thick multifunctional cardiac patches. P Natl Acad Sci USA. 114(8), 1898–1903 (2017). https://doi.org/10.1073/pnas.1615728114

    Article  Google Scholar 

  130. Richards, D.J., Coyle, R.C., Tan, Y., Jia, J., Wong, K., Toomer, K., et al.: Inspiration from heart development: biomimetic development of functional human cardiac organoids. Biomaterials. 142, 112–123 (2017). https://doi.org/10.1016/j.biomaterials.2017.07.021

    Article  Google Scholar 

Download references

Acknowledgement

The authors acknowledge the grant support from NIH NICHD (R01HD101130) and NIAMS (R21AR076645), NSF (CBET-1804875 and CBET-1943798) and Syracuse University intramural CUSE Grant, Gerber Grant and BioInspired Institute Seed Grant.

Author information

Authors and Affiliations

  1. Department of Biomedical and Chemical Engineering, Syracuse University, Syracuse, NY, USA

    Chenyan Wang & Zhen Ma

  2. BioInspired Syracuse: Institute for Material and Living Systems, Syracuse University, Syracuse, NY, USA

    Chenyan Wang & Zhen Ma

Authors
  1. Chenyan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhen Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhen Ma .

Editor information

Editors and Affiliations

  1. Biomedical Engineering, University of Alabama at Birmingham, Birmingham, AL, USA

    Jianyi Zhang

  2. Biomedical Engineering, Georgia Institute of Technology, Atlanta, GA, USA

    Vahid Serpooshan

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Wang, C., Ma, Z. (2022). Biomaterial Interface in Cardiac Cell and Tissue Engineering. In: Zhang, J., Serpooshan, V. (eds) Advanced Technologies in Cardiovascular Bioengineering. Springer, Cham. https://doi.org/10.1007/978-3-030-86140-7_12

Download citation

  • DOI: https://doi.org/10.1007/978-3-030-86140-7_12

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-030-86139-1

  • Online ISBN: 978-3-030-86140-7

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics

Search

Navigation