1932

Abstract

Engineered, in vitro cardiac cell and tissue systems provide test beds for the study of cardiac development, cellular disease processes, and drug responses in a dish. Much effort has focused on improving the structure and function of engineered cardiomyocytes and heart tissues. However, these parameters depend critically on signaling through the cellular microenvironment in terms of ligand composition, matrix stiffness, and substrate mechanical properties—that is, matrix micromechanobiology. To facilitate improvements to in vitro microenvironment design, we review how cardiomyocytes and their microenvironment change during development and disease in terms of integrin expression and extracellular matrix (ECM) composition. We also discuss strategies used to bind proteins to common mechanobiology platforms and describe important differences in binding strength to the substrate. Finally, we review example biomaterial approaches designed to support and probe cell–ECM interactions of cardiomyocytes in vitro, as well as open questions and challenges.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-092019-034950
2020-06-04
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/bioeng/22/1/annurev-bioeng-092019-034950.html?itemId=/content/journals/10.1146/annurev-bioeng-092019-034950&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Bowers SLK, McFadden WA, Borg TK, Baudino TA 2012. Desmoplakin is important for proper cardiac cell–cell interactions. Microsc. Microanal. 18:107–14
    [Google Scholar]
  2. 2. 
    Rienks M, Papageorgiou A-P, Frangogiannis NG, Heymans S 2014. Myocardial extracellular matrix: an ever-changing and diverse entity. Circ. Res. 114:872–88
    [Google Scholar]
  3. 3. 
    Simmons CS, Petzold BC, Pruitt BL 2012. Microsystems for biomimetic stimulation of cardiac cells. Lab Chip 12:3235–48
    [Google Scholar]
  4. 4. 
    Zak R. 1973. Cell proliferation during cardiac growth. Am. J. Cardiol. 31:211–19
    [Google Scholar]
  5. 5. 
    Später D, Hansson EM, Zangi L, Chien KR 2014. How to make a cardiomyocyte. Development 141:4418–31
    [Google Scholar]
  6. 6. 
    De Franceschi N, Hamidi H, Alanko J, Sahgal P, Ivaskà J 2015. Integrin traffic—the update. J. Cell Sci. 128:839–52
    [Google Scholar]
  7. 7. 
    Frantz C, Stewart KM, Weaver VM 2010. The extracellular matrix at a glance. J. Cell Sci. 123:4195–200
    [Google Scholar]
  8. 8. 
    Hynes RO. 2009. The extracellular matrix: not just pretty fibrils. Science 326:1216–19
    [Google Scholar]
  9. 9. 
    Israeli-Rosenberg S, Manso AM, Okada H, Ross RS 2014. Integrins and integrin-associated proteins in the cardiac myocyte. Circ. Res. 114:572–86
    [Google Scholar]
  10. 10. 
    Michele DE, Kabaeva Z, Davis SL, Weiss RM, Campbell KP 2009. Dystroglycan matrix receptor function in cardiac myocytes is important for limiting activity-induced myocardial damage. Circ. Res. 105:984–93
    [Google Scholar]
  11. 11. 
    Adams JC, Brancaccio A. 2015. The evolution of the dystroglycan complex, a major mediator of muscle integrity. Biol. Open 4:1163–79
    [Google Scholar]
  12. 12. 
    Xie J, He G, Chen Q, Sun J, Dai Q et al. 2016. Syndecan-4 signaling is required for exercise-induced cardiac hypertrophy. Mol. Med. 22:192–201
    [Google Scholar]
  13. 13. 
    Peter AK, Cheng H, Ross RS, Knowlton KU, Chen J 2011. The costamere bridges sarcomeres to the sarcolemma in striated muscle. Prog. Pediatr. Cardiol. 31:83–88
    [Google Scholar]
  14. 14. 
    Samarel AM. 2005. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am. J. Physiol. Heart Circ. Physiol. 298:H2291–301
    [Google Scholar]
  15. 15. 
    Baldwin HS, Buck CA. 1994. Integrins and other cell adhesion molecules in cardiac development. Trends Cardiovasc. Med. 4:178–87
    [Google Scholar]
  16. 16. 
    Forbes MS, Sperelakis N. 1985. Intercalated discs of mammalian heart: a review of structure and function. Tissue Cell 17:605–48
    [Google Scholar]
  17. 17. 
    Ross RS, Borg TK. 2001. Integrins and the myocardium. Circ. Res. 88:1112–19
    [Google Scholar]
  18. 18. 
    Huveneers S, Danen EHJ. 2009. Adhesion signaling—crosstalk between integrins, Src and Rho. J. Cell Sci. 122:1059–69
    [Google Scholar]
  19. 19. 
    Humphries JD, Chastney MR, Askari JA, Humphries MJ 2019. Signal transduction via integrin adhesion complexes. Curr. Opin. Cell Biol. 56:14–21
    [Google Scholar]
  20. 20. 
    Lundgren E, Gullberg D, Rubin K, Borg TK, Terracio MJ, Terracio L 1988. In vitro studies on adult cardiac myocytes: attachment and biosynthesis of collagen type IV and laminin. J. Cell. Physiol. 136:43–53
    [Google Scholar]
  21. 21. 
    Mott JD, Werb Z. 2004. Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 16:558–64
    [Google Scholar]
  22. 22. 
    Miner EC, Miller WL. 2006. A look between the cardiomyocytes: the extracellular matrix in heart failure. Mayo Clin. Proc. 81:71–76
    [Google Scholar]
  23. 23. 
    Mishra PK, Givvimani S, Chavali V, Tyagi SC 2013. Cardiac matrix: a clue for future therapy. Biochim. Biophys. Acta Mol. Basis Dis. 1832:2271–76
    [Google Scholar]
  24. 24. 
    Barczyk M, Carracedo S, Gullberg D 2010. Integrins. Cell Tissue Res 339:269–80
    [Google Scholar]
  25. 25. 
    Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T et al. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–72
    [Google Scholar]
  26. 26. 
    Gherghiceanu M, Barad L, Novak A, Reiter I, Itskovitz-Eldor J et al. 2011. Cardiomyocytes derived from human embryonic and induced pluripotent stem cells: comparative ultrastructure. J. Cell. Mol. Med. 15:2539–51
    [Google Scholar]
  27. 27. 
    Yang X, Pabon L, Murry CE 2014. Engineering adolescence: maturation of human pluripotent stem cell–derived cardiomyocytes. Circ. Res. 114:511–23
    [Google Scholar]
  28. 28. 
    Scuderi GJ, Butcher J. 2017. Naturally engineered maturation of cardiomyocytes. Front. Cell Dev. Biol. 5:50
    [Google Scholar]
  29. 29. 
    Milani-Nejad N, Janssen PML. 2014. Small and large animal models in cardiac contraction research: advantages and disadvantages. Pharmacol. Ther. 141:235–49
    [Google Scholar]
  30. 30. 
    Spudich JA. 2014. Hypertrophic and dilated cardiomyopathy: Four decades of basic research on muscle lead to potential therapeutic approaches to these devastating genetic diseases. Biophys. J. 106:1236–49
    [Google Scholar]
  31. 31. 
    Kolanowski TJ, Antos CL, Guan K 2017. Making human cardiomyocytes up to date: derivation, maturation state and perspectives. Int. J. Cardiol. 241:379–86
    [Google Scholar]
  32. 32. 
    Yang X, Pabon L, Murry CE 2014. Engineering adolescence. Circ. Res. 114:511–23
    [Google Scholar]
  33. 33. 
    Lundy SD, Zhu W-Z, Regnier M, Laflamme MA 2013. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev 22:1991–2002
    [Google Scholar]
  34. 34. 
    Ronaldson-Bouchard K, Ma SP, Yeager K, Chen T, Song L et al. 2018. Advanced maturation of human cardiac tissue grown from pluripotent stem cells. Nature 556:239–43
    [Google Scholar]
  35. 35. 
    Liu AP, Chaudhuri O, Parekh SH 2017. New advances in probing cell–extracellular matrix interactions. Integr. Biol. 9:383–405
    [Google Scholar]
  36. 36. 
    Darnell M, Mooney DJ. 2017. Leveraging advances in biology to design biomaterials. Nat. Mater. 16:1178–85
    [Google Scholar]
  37. 37. 
    Campbell ID, Humphries MJ. 2011. Integrin structure, activation, and interactions. Cold Spring Harb. Perspect. Biol. 3:a004994
    [Google Scholar]
  38. 38. 
    Humphries JD, Byron A, Humphries MJ 2006. Integrin ligands at a glance. J. Cell Sci. 119:3901–3
    [Google Scholar]
  39. 39. 
    Roca-Cusachs P, Gauthier NC, Del Rio A, Sheetz MP 2009. Clustering of α5β1 integrins determines adhesion strength whereas αVβ3 and talin enable mechanotransduction. PNAS 106:16245–50
    [Google Scholar]
  40. 40. 
    Balcioglu HE, van Hoorn H, Donato DM, Schmidt T, Danen EHJ 2015. The integrin expression profile modulates orientation and dynamics of force transmission at cell–matrix adhesions. J. Cell Sci. 128:1316–26
    [Google Scholar]
  41. 41. 
    Kechagia JZ, Ivaska J, Roca-Cusachs P 2019. Integrins as biomechanical sensors of the microenvironment. Nat. Rev. Mol. Cell Biol. 20:457–73
    [Google Scholar]
  42. 42. 
    Vogel C, Marcotte EM. 2012. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13:227–32
    [Google Scholar]
  43. 43. 
    Meliopoulos VA, Schultz-Cherry S. 2018. Although it's painful: the importance of stringent antibody validation. PLOS Pathog 14:e1006701
    [Google Scholar]
  44. 44. 
    Chen C, Li R, Ross RS, Manso AM 2016. Integrins and integrin-related proteins in cardiac fibrosis. J. Mol. Cell. Cardiol. 93:162–74
    [Google Scholar]
  45. 45. 
    Brancaccio M, Cabodi S, Belkin AM, Collo G, Koteliansky VE et al. 1998. Differential onset of expression of alpha 7 and beta 1D integrins during mouse heart and skeletal muscle development. Cell Adhes. Commun. 5:193–205
    [Google Scholar]
  46. 46. 
    Wiencierz AM, Kernbach M, Ecklebe J, Monnerat G, Tomiuk S et al. 2015. Differential expression levels of integrin α6 enable the selective identification and isolation of atrial and ventricular cardiomyocytes. PLOS ONE 10:e0143538
    [Google Scholar]
  47. 47. 
    Humphries JD, Byron A, Humphries MJ 2006. Integrin ligands at a glance. J. Cell Sci. 119:3901–3
    [Google Scholar]
  48. 48. 
    Terracio L, Rubin K, Gullberg D, Balog E, Carver W et al. 1991. Expression of collagen binding integrins during cardiac development and hypertrophy. Circ. Res. 68:734–44
    [Google Scholar]
  49. 49. 
    Nawata J, Ohno I, Isoyama S, Suzuki J, Miura S et al. 1999. Differential expression of α1, α3 and α5 integrin subunits in acute and chronic stages of myocardial infarction in rats. Cardiovasc. Res. 43:371–81
    [Google Scholar]
  50. 50. 
    Domogatskaya A, Rodin S, Tryggvason K 2012. Functional diversity of laminins. Annu. Rev. Cell Dev. Biol. 28:523–53
    [Google Scholar]
  51. 51. 
    Babbitt CJ, Shai S-Y, Harpf AE, Pham CG, Ross RS 2002. Modulation of integrins and integrin signaling molecules in the pressure-loaded murine ventricle. Histochem. Cell Biol. 118:431–39
    [Google Scholar]
  52. 52. 
    Van Der Flier A, Gaspar AC, Thorsteinsdóttir S, Baudoin C, Groeneveld E et al. 1997. Spatial and temporal expression of the β1D integrin during mouse development. Dev. Dyn. 210:472–86
    [Google Scholar]
  53. 53. 
    Belkin AM, Zhidkova NI, Balzac F, Altruda F, Tomatis D et al. 1996. Beta 1D integrin displaces the beta 1A isoform in striated muscles: localization at junctional structures and signaling potential in nonmuscle cells. J. Cell Biol. 132:211–26
    [Google Scholar]
  54. 54. 
    Sun M, Opavsky MA, Stewart DJ, Rabinovitch M, Dawood F et al. 2003. Temporal response and localization of integrins β1 and β3 in the heart after myocardial infarction. Circulation 107:1046–52
    [Google Scholar]
  55. 55. 
    Krishnamurthy P, Subramanian V, Singh M, Singh K 2006. Deficiency of β1 integrins results in increased myocardial dysfunction after myocardial infarction. Heart 92:1309–15
    [Google Scholar]
  56. 56. 
    Ichikawa Y, Zemljic-Harpf AE, Zhang Z, McKirnan MD, Manso AM et al. 2017. Modulation of caveolins, integrins and plasma membrane repair proteins in anthracycline-induced heart failure in rabbits. PLOS ONE 12:e0177660
    [Google Scholar]
  57. 57. 
    Manso AM, Okada H, Sakamoto FM, Moreno E, Monkley SJ et al. 2017. Loss of mouse cardiomyocyte talin-1 and talin-2 leads to β-1 integrin reduction, costameric instability, and dilated cardiomyopathy. PNAS 114:E6250–59
    [Google Scholar]
  58. 58. 
    Schips TG, Vanhoutte D, Vo A, Correll RN, Brody MJ et al. 2019. Thrombospondin-3 augments injury-induced cardiomyopathy by intracellular integrin inhibition and sarcolemmal instability. Nat. Commun. 10:76
    [Google Scholar]
  59. 59. 
    Rowland TJ, Miller LM, Blaschke AJ, Doss EL, Bonham AJ et al. 2010. Roles of integrins in human induced pluripotent stem cell growth on Matrigel and vitronectin. Stem Cells Dev 19:1231–40
    [Google Scholar]
  60. 60. 
    Ja KPMM, Miao Q, Zhen Tee NG, Lim SY, Nandihalli M et al. 2016. iPSC-derived human cardiac progenitor cells improve ventricular remodelling via angiogenesis and interstitial networking of infarcted myocardium. J. Cell. Mol. Med. 20:323–32
    [Google Scholar]
  61. 61. 
    Yu T, Miyagawa S, Miki K, Saito A, Fukushima S et al. 2013. In vivo differentiation of induced pluripotent stem cell–derived cardiomyocytes. Circ. J. 77:1297–306
    [Google Scholar]
  62. 62. 
    Karpievitch YV, Polpitiya AD, Anderson GA, Smith RD, Dabney AR 2010. Liquid chromatography mass spectrometry–based proteomics: biological and technological aspects. Ann. Appl. Stat. 4:1797–823
    [Google Scholar]
  63. 63. 
    Schmuck EG, Hematti P, Raval AN 2018. Cardiac Extracellular Matrix Fundamental Science to Clinical Applications Cham, Switz.: Springer
  64. 64. 
    Chang CW, Dalgliesh AJ, López JE, Griffiths LG 2016. Cardiac extracellular matrix proteomics: challenges, techniques, and clinical implications. Proteom. Clin. Appl. 10:39–50
    [Google Scholar]
  65. 65. 
    Schwach V, Passier R. 2019. Native cardiac environment and its impact on engineering cardiac tissue. Biomater. Sci. 7:3566–80
    [Google Scholar]
  66. 66. 
    de Souza RR. 2002. Aging of myocardial collagen. Biogerontology 3:325–35
    [Google Scholar]
  67. 67. 
    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. 70:1006–17
    [Google Scholar]
  68. 68. 
    Fomovsky GM, Thomopoulos S, Holmes JW 2010. Contribution of extracellular matrix to the mechanical properties of the heart. J. Mol. Cell. Cardiol. 48:490–96
    [Google Scholar]
  69. 69. 
    Speiser B, Riess CF, Schaper J 1991. The extracellular matrix in human myocardium. Part I: Collagens I, III, IV, and VI. Cardioscience 2:225–32
    [Google Scholar]
  70. 70. 
    Hanson KP, Jung JP, Tran QA, Hsu S-PP, Iida R et al. 2013. Spatial and temporal analysis of extracellular matrix proteins in the developing murine heart: a blueprint for regeneration. Tissue Eng. A 19:1132–43
    [Google Scholar]
  71. 71. 
    Marijianowski MMH, van der Loos CM, Mohrschladt MF, Becker AE 1994. The neonatal heart has a relatively high content of total collagen and type I collagen, a condition that may explain the less compliant state. J. Am. Coll. Cardiol. 23:1204–8
    [Google Scholar]
  72. 72. 
    Borg TK, Gay RE, Johnson LD 1982. Changes in the distribution of fibronectin and collagen during development of the neonatal rat heart. Coll. Relat. Res. 2:211–18
    [Google Scholar]
  73. 73. 
    Gershlak JR, Resnikoff JI, Sullivan KE, Williams C, Wang RM, Black LD III 2013. Mesenchymal stem cells ability to generate traction stress in response to substrate stiffness is modulated by the changing extracellular matrix composition of the heart during development. Biochem. Biophys. Res. Commun. 439:161–66
    [Google Scholar]
  74. 74. 
    Williams C, Quinn KP, Georgakoudi I, Black LD III 2014. Young developmental age cardiac extracellular matrix promotes the expansion of neonatal cardiomyocytes in vitro. Acta Biomater 10:194–204
    [Google Scholar]
  75. 75. 
    Wei S, Chow LTC, Shum IOL, Qin L, Sanderson JE 1999. Left and right ventricular collagen type I/III ratios and remodeling post-myocardial infarction. J. Card. Fail. 5:117–26
    [Google Scholar]
  76. 76. 
    Sullivan KE, Quinn KP, Tang KM, Georgakoudi I, Black LD III 2014. Extracellular matrix remodeling following myocardial infarction influences the therapeutic potential of mesenchymal stem cells. Stem Cell Res. Ther. 5:14
    [Google Scholar]
  77. 77. 
    Quinn KP, Sullivan KE, Liu Z, Ballard Z, Siokatas C et al. 2016. Optical metrics of the extracellular matrix predict compositional and mechanical changes after myocardial infarction. Sci. Rep. 6:35823
    [Google Scholar]
  78. 78. 
    Yang H, Borg TK, Liu H, Gao BZ 2015. Interactive relationship between basement-membrane development and sarcomerogenesis in single cardiomyocytes. Exp. Cell Res. 330:222–32
    [Google Scholar]
  79. 79. 
    Luther DJ, Thodeti CK, Shamhart PE, Adapala RK, Hodnichak C et al. 2012. Absence of type VI collagen paradoxically improves cardiac function, structure, and remodeling after myocardial infarction. Circ. Res. 110:851–56
    [Google Scholar]
  80. 80. 
    Rasi K, Piuhola J, Czabanka M, Sormunen R, Ilves M et al. 2010. Collagen XV is necessary for modeling of the extracellular matrix and its deficiency predisposes to cardiomyopathy. Circ. Res. 107:1241–52
    [Google Scholar]
  81. 81. 
    Jourdan-LeSaux C, Zhang J, Lindsey ML 2010. Extracellular matrix roles during cardiac repair. Life Sci 87:391–400
    [Google Scholar]
  82. 82. 
    Boateng SY, Lateef SS, Mosley W, Hartman TJ, Hanley L, Russell B 2005. RGD and YIGSR synthetic peptides facilitate cellular adhesion identical to that of laminin and fibronectin but alter the physiology of neonatal cardiac myocytes. Am. J. Physiol. Cell Physiol. 288:C30–38
    [Google Scholar]
  83. 83. 
    Roediger M, Miosge N, Gersdorff N 2010. Tissue distribution of the laminin β1 and β2 chain during embryonic and fetal human development. J. Mol. Histol. 41:177–84
    [Google Scholar]
  84. 84. 
    Yap L, Wang J-W, Moreno-Moral A, Chong LY, Sun Y et al. 2019. In vivo generation of post-infarct human cardiac muscle by laminin-promoted cardiovascular progenitors. Cell Rep 26:3231–45
    [Google Scholar]
  85. 85. 
    Ulrich MMW, Janssen AMH, Daemen MJAP, Rappaport L, Samuel J-L et al. 1997. Increased expression of fibronectin isoforms after myocardial infarction in rats. J. Mol. Cell Cardiol. 29:2533–43
    [Google Scholar]
  86. 86. 
    Linask KK, Lash JW. 1988. A role for fibronectin in the migration of avian precardiac cells. II. Rotation of the heart-forming region during different stages and its effects. Dev. Biol. 129:324–29
    [Google Scholar]
  87. 87. 
    van Dijk A, Niessen HWM, Ursem W, Twisk JWR, Visser FC, van Milligen FJ 2008. Accumulation of fibronectin in the heart after myocardial infarction: a putative stimulator of adhesion and proliferation of adipose-derived stem cells. Cell Tissue Res 332:289–98
    [Google Scholar]
  88. 88. 
    Balasubramanian S, Quinones L, Kasiganesan H, Zhang Y, Pleasant DL 2012. β3 integrin in cardiac fibroblast is critical for extracellular matrix accumulation during pressure overload hypertrophy in mouse. PLOS ONE 7:e45076
    [Google Scholar]
  89. 89. 
    Ramos IT, Henningsson M, Nezafat M, Lavin B, Lorrio S et al. 2018. Simultaneous assessment of cardiac inflammation and extracellular matrix remodeling after myocardial infarction. Circ. Cardiovasc. Imaging 11:e007453
    [Google Scholar]
  90. 90. 
    Lee JP, Kassianidou E, MacDonald JI, Francis MB, Kumar S 2016. N-terminal specific conjugation of extracellular matrix proteins to 2-pyridinecarboxaldehyde functionalized polyacrylamide hydrogels. Biomaterials 102:268–76
    [Google Scholar]
  91. 91. 
    Halldorsson S, Lucumi E, Gómez-Sjöberg R, Fleming RMT 2015. Advantages and challenges of microfluidic cell culture in polydimethylsiloxane devices. Biosens. Bioelectron. 63:218–31
    [Google Scholar]
  92. 92. 
    Damljanović V, Lagerholm BC, Jacobson K 2005. Bulk and micropatterned conjugation of extracellular matrix proteins to characterized polyacrylamide substrates for cell mechanotransduction assays. Biotechniques 39:847–51
    [Google Scholar]
  93. 93. 
    Nelson CM, Raghavan S, Tan JL, Chen CS 2003. Degradation of micropatterned surfaces by cell-dependent and -independent processes. Langmuir 19:1493–99
    [Google Scholar]
  94. 94. 
    Tang X, Yakut Ali M, Saif MTA 2012. A novel technique for micro-patterning proteins and cells on polyacrylamide gels. Soft Matter 8:7197–206
    [Google Scholar]
  95. 95. 
    Moeller J, Denisin AK, Sim JY, Wilson RE, Ribeiro AJS, Pruitt BL 2018. Controlling cell shape on hydrogels using lift-off protein patterning. PLOS ONE 13:e0189901
    [Google Scholar]
  96. 96. 
    Ribeiro AJS, Denisin AK, Wilson RE, Pruitt BL 2016. For whom the cells pull: hydrogel and micropost devices for measuring traction forces. Methods 94:51–64
    [Google Scholar]
  97. 97. 
    Pelham RJ, Wang Y-L. 1997. Cell locomotion and focal adhesions are regulated by substrate flexibility. PNAS 94:13661–65
    [Google Scholar]
  98. 98. 
    Lekka M, Pabijan J, Orzechowska B 2019. Morphological and mechanical stability of bladder cancer cells in response to substrate rigidity. Biochim. Biophys. Acta Gen. Subj. 1863:1006–14
    [Google Scholar]
  99. 99. 
    Wen JH, Vincent LG, Fuhrmann A, Choi YS, Hribar K et al. 2014. Interplay of matrix stiffness and protein tethering in stem cell differentiation. Nat. Mater. 13:979–87
    [Google Scholar]
  100. 100. 
    Dembo M, Wang YL. 1999. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76:2307–16
    [Google Scholar]
  101. 101. 
    Charrier EE, Pogoda K, Wells RG, Janmey PA 2018. Control of cell morphology and differentiation by substrates with independently tunable elasticity and viscous dissipation. Nat. Commun. 9:449
    [Google Scholar]
  102. 102. 
    Reinhart-King CA, Dembo M, Hammer DA 2005. The dynamics and mechanics of endothelial cell spreading. Biophys. J. 89:676–89
    [Google Scholar]
  103. 103. 
    Macdonald JI, Munch HK, Moore T, Francis MB 2015. One-step site-specific modification of native proteins with 2-pyridinecarboxyaldehydes. Nat. Chem. Biol. 11:326–31
    [Google Scholar]
  104. 104. 
    Gokaltun A, Yarmush ML, Asatekin A, Usta OB 2017. Recent advances in nonbiofouling PDMS surface modification strategies applicable to microfluidic technology. Technology 5:1–12
    [Google Scholar]
  105. 105. 
    Khnouf R, Karasneh D, Albiss BA 2016. Protein immobilization on the surface of polydimethylsiloxane and polymethyl methacrylate microfluidic devices. Electrophoresis 37:529–35
    [Google Scholar]
  106. 106. 
    De Silva MN, Desai R, Odde DJ 2004. Micro-patterning of animal cells on PDMS substrates in the presence of serum without use of adhesion inhibitors. Biomed. Microdevices 6:219–22
    [Google Scholar]
  107. 107. 
    Eteshola E, Leckband D. 2001. Development and characterization of an ELISA assay in PDMS microfluidic channels. Sens. Actuators B 72:129–33
    [Google Scholar]
  108. 108. 
    Mobasseri SA, Zijl S, Salameti V, Walko G, Stannard A et al. 2019. Patterning of human epidermal stem cells on undulating elastomer substrates reflects differences in cell stiffness. Acta Biomater 87:256–64
    [Google Scholar]
  109. 109. 
    Kim Y, Kwon C, Jeon H 2017. Genetically engineered phage induced selective H9c2 cardiomyocytes patterning in PDMS microgrooves. Materials 10:E973
    [Google Scholar]
  110. 110. 
    Ferguson GS, Chaudhury MK, Biebuyck HA, Whitesides GM 1993. Monolayers on disordered substrates: self-assembly of alkyltrichlorosilanes on surface-modified polyethylene and poly(dimethylsiloxane). Macromolecules 26:5870–75
    [Google Scholar]
  111. 111. 
    Chaudhury MK, Whitesides GM. 1991. Direct measurement of interfacial interactions between semispherical lenses and flat sheets of poly(dimethylsiloxane) and their chemical derivatives. Langmuir 7:1013–25
    [Google Scholar]
  112. 112. 
    Zhang W, Choi DS, Nguyen YH, Chang J, Qin L 2013. Studying cancer stem cell dynamics on PDMS surfaces for microfluidics device design. Sci. Rep. 3:2332
    [Google Scholar]
  113. 113. 
    Yang Y, Kulangara K, Lam RTS, Dharmawan R, Leong KW 2012. Effects of topographical and mechanical property alterations induced by oxygen plasma modification on stem cell behavior. ACS Nano 6:8591–98
    [Google Scholar]
  114. 114. 
    Nam KH, Jamilpour N, Mfoumou E, Wang FY, Zhang DD, Wong PK 2014. Probing mechanoregulation of neuronal differentiation by plasma lithography patterned elastomeric substrates. Sci. Rep. 4:6965
    [Google Scholar]
  115. 115. 
    Farrell M, Beaudoin S. 2010. Surface forces and protein adsorption on dextran- and polyethylene glycol–modified polydimethylsiloxane. Colloids Surfaces B 81:468–75
    [Google Scholar]
  116. 116. 
    Hu S, Chen TH, Zhao Y, Wang Z, Lam RHW 2018. Protein–substrate adhesion in microcontact printing regulates cell behavior. Langmuir 34:1750–59
    [Google Scholar]
  117. 117. 
    Kuddannaya S, Chuah YJ, Lee MHA, Menon NV, Kang Y, Zhang Y 2013. Surface chemical modification of poly(dimethylsiloxane) for the enhanced adhesion and proliferation of mesenchymal stem cells. ACS Appl. Mater. Interfaces 5:9777–84
    [Google Scholar]
  118. 118. 
    Leivo J, Kartasalo K, Kallio P, Virjula S, Miettinen S et al. 2017. A durable and biocompatible ascorbic acid–based covalent coating method of polydimethylsiloxane for dynamic cell culture. J. R. Soc. Interface 14:20170318
    [Google Scholar]
  119. 119. 
    Huang B, Wu H, Kim S, Kobilka BK, Zare RN 2006. Phospholipid biotinylation of polydimethylsiloxane (PDMS) for protein immobilization. Lab Chip 6:369–73
    [Google Scholar]
  120. 120. 
    Wang RM, Christman KL. 2016. Decellularized myocardial matrix hydrogels: in basic research and preclinical studies. Adv. Drug Deliv. Rev. 96:77–82
    [Google Scholar]
  121. 121. 
    Santoro R, Perrucci GL, Gowran A, Pompilio G 2019. Unchain my heart: integrins at the basis of iPSC cardiomyocyte differentiation. Stem Cells Int 2019:1–20
    [Google Scholar]
  122. 122. 
    Bejleri D, Davis ME. 2019. Decellularized extracellular matrix materials for cardiac repair and regeneration. Adv. Healthc. Mater. 8:1801217
    [Google Scholar]
  123. 123. 
    Taylor DA, Parikh RB, Sampaio LC 2017. Bioengineering hearts: simple yet complex. Curr. Stem Cell Rep. 3:35–44
    [Google Scholar]
  124. 124. 
    Paoletti C, Divieto C, Chiono V 2018. Impact of biomaterials on differentiation and reprogramming approaches for the generation of functional cardiomyocytes. Cells 7:E114
    [Google Scholar]
  125. 125. 
    Chen QZ, Harding SE, Ali NN, Lyon AR, Boccaccini AR 2008. Biomaterials in cardiac tissue engineering: ten years of research survey. Mater. Sci. Eng. R 59:1–37
    [Google Scholar]
  126. 126. 
    Segers VFM, Lee RT. 2011. Biomaterials to enhance stem cell function in the heart. Circ. Res. 109:910–22
    [Google Scholar]
  127. 127. 
    Borg TK, Rubin K, Lundgren E, Borg K, Öbrink B 1984. Recognition of extracellular matrix components by neonatal and adult cardiac myocytes. Dev. Biol. 104:86–96
    [Google Scholar]
  128. 128. 
    Burridge PW, Matsa E, Shukla P, Lin ZC, Churko JM et al. 2014. Chemically defined generation of human cardiomyocytes. Nat. Methods 11:855–60
    [Google Scholar]
  129. 129. 
    Hirata N, Nakagawa M, Fujibayashi Y, Yamauchi K, Murata A et al. 2014. A chemical probe that labels human pluripotent stem cells. Cell Rep 6:1165–74
    [Google Scholar]
  130. 130. 
    Patel AK, Celiz AD, Rajamohan D, Anderson DG, Langer R et al. 2015. A defined synthetic substrate for serum-free culture of human stem cell derived cardiomyocytes with improved functional maturity identified using combinatorial materials microarrays. Biomaterials 61:257–65
    [Google Scholar]
  131. 131. 
    Battista S, Guarnieri D, Borselli C, Zeppetelli S, Borzacchiello A et al. 2005. The effect of matrix composition of 3D constructs on embryonic stem cell differentiation. Biomaterials 26:6194–207
    [Google Scholar]
  132. 132. 
    Jung JP, Hu D, Domian IJ, Ogle BM 2015. An integrated statistical model for enhanced murine cardiomyocyte differentiation via optimized engagement of 3D extracellular matrices. Sci. Rep. 5:18705
    [Google Scholar]
  133. 133. 
    Discher DE, Janmey P, Wang Y 2005. Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139–43
    [Google Scholar]
  134. 134. 
    Corbin EA, Vite A, Peyster EG, Bhoopalam M, Brandimarto J et al. 2019. Tunable and reversible substrate stiffness reveals a dynamic mechanosensitivity of cardiomyocytes. ACS Appl. Mater. Interfaces 11:20603–14
    [Google Scholar]
  135. 135. 
    Young JL, Engler AJ. 2011. Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro. Biomaterials 32:1002–9
    [Google Scholar]
  136. 136. 
    Majkut S, Idema T, Swift J, Krieger C, Liu A, Discher DE 2013. Heart-specific stiffening in early embryos parallels matrix and myosin expression to optimize beating. Curr. Biol. 23:2434–39
    [Google Scholar]
  137. 137. 
    Berry MF, Engler AJ, Woo YJ, Pirolli TJ, Bish LT et al. 2006. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart Circ. Physiol. 290:H2196–203
    [Google Scholar]
  138. 138. 
    Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang H-Y et al. 2008. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: Scar-like rigidity inhibits beating. J. Cell Sci. 121:3794–802
    [Google Scholar]
  139. 139. 
    Chung C, Anderson E, Pera RR, Pruitt BL, Heilshorn SC 2012. Hydrogel crosslinking density regulates temporal contractility of human embryonic stem cell–derived cardiomyocytes in 3D cultures. Soft Matter 8:10141–48
    [Google Scholar]
  140. 140. 
    Hirata M, Yamaoka T. 2018. Effect of stem cell niche elasticity/ECM protein on the self-beating cardiomyocyte differentiation of induced pluripotent stem (iPS) cells at different stages. Acta Biomater 65:44–52
    [Google Scholar]
  141. 141. 
    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 181:280–92
    [Google Scholar]
  142. 142. 
    Branco MA, Cotovio JP, Rodrigues CAV, Vaz SH, Fernandes TG et al. 2019. Transcriptomic analysis of 3D cardiac differentiation of human induced pluripotent stem cells reveals faster cardiomyocyte maturation compared to 2D culture. Sci. Rep. 9:9229
    [Google Scholar]
  143. 143. 
    Kerscher P, Turnbull IC, Hodge AJ, Kim J, Seliktar D et al. 2016. Direct hydrogel encapsulation of pluripotent stem cells enables ontomimetic differentiation and growth of engineered human heart tissues. Biomaterials 83:383–95
    [Google Scholar]
  144. 144. 
    Zhang D, Shadrin IY, Lam J, Xian HQ, Snodgrass HR, Bursac N 2013. Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34:5813–20
    [Google Scholar]
  145. 145. 
    Lemoine MD, Mannhardt I, Breckwoldt K, Prondzynski M, Flenner F et al. 2017. Human iPSC-derived cardiomyocytes cultured in 3D engineered heart tissue show physiological upstroke velocity and sodium current density. Sci. Rep. 7:5464
    [Google Scholar]
  146. 146. 
    Carson D, Hnilova M, Yang X, Nemeth CL, Tsui JH et al. 2016. Nanotopography-induced structural anisotropy and sarcomere development in human cardiomyocytes derived from induced pluripotent stem cells. ACS Appl. Mater. Interfaces 8:21923–32
    [Google Scholar]
  147. 147. 
    Seo HR, Joo HJ, Kim DH, Cui LH, Choi SC et al. 2017. Nanopillar surface topology promotes cardiomyocyte differentiation through cofilin-mediated cytoskeleton rearrangement. ACS Appl. Mater. Interfaces 9:16803–12
    [Google Scholar]
  148. 148. 
    Abadi PPSS, Garbern JC, Behzadi S, Hill MJ, Tresback JS et al. 2018. Engineering of mature human induced pluripotent stem cell–derived cardiomyocytes using substrates with multiscale topography. Adv. Funct. Mater. 28:1–11
    [Google Scholar]
  149. 149. 
    Chen H, Song W, Zhou F, Wu Z, Huang H et al. 2009. The effect of surface microtopography of poly(dimethylsiloxane) on protein adsorption, platelet and cell adhesion. Colloids Surf. B 71:275–81
    [Google Scholar]
  150. 150. 
    Delcommenne M, Streuli CH. 1995. Control of integrin expression by extracellular matrix. J. Biol. Chem. 270:26794–801
    [Google Scholar]
  151. 151. 
    Vite A, Radice GL. 2014. N-Cadherin/catenin complex as a master regulator of intercalated disc function. Cell Commun. Adhes. 21:169–79
    [Google Scholar]
  152. 152. 
    McCain ML, Lee H, Aratyn-Schaus Y, Kléber AG, Parker KK 2012. Cooperative coupling of cell–matrix and cell–cell adhesions in cardiac muscle. PNAS 109:9881–86
    [Google Scholar]
  153. 153. 
    Chopra A, Tabdanov E, Patel H, Janmey PA, Kresh JY 2011. Cardiac myocyte remodeling mediated by N-cadherin-dependent mechanosensing. Am. J. Physiol. Heart Circ. Physiol. 300:H1252–66
    [Google Scholar]
  154. 154. 
    Nitsan I, Drori S, Lewis YE, Cohen S, Tzlil S 2016. Mechanical communication in cardiac cell synchronized beating. Nat. Phys. 12:472–77
    [Google Scholar]
  155. 155. 
    Marsico G, Russo L, Quondamatteo F, Pandit A 2018. Glycosylation and integrin regulation in cancer. Trends Cancer 4:537–52
    [Google Scholar]
  156. 156. 
    Seetharaman S, Etienne-Manneville S. 2018. Integrin diversity brings specificity in mechanotransduction. Biol. Cell 110:49–64
    [Google Scholar]
  157. 157. 
    Berk BC, Fujiwara K, Lehoux S 2007. ECM remodeling in hypertensive heart disease. J. Clin. Investig. 117:568–75
    [Google Scholar]
/content/journals/10.1146/annurev-bioeng-092019-034950
Loading
/content/journals/10.1146/annurev-bioeng-092019-034950
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error