Mechanotransduction: the role of mechanical stress, myocyte shape, and cytoskeletal architecture on cardiac function

  • Megan L. McCain
  • Kevin Kit ParkerEmail author
Invited Review


Mechanotransduction refers to the conversion of mechanical forces into biochemical or electrical signals that initiate structural and functional remodeling in cells and tissues. The heart is a kinetic organ whose form changes considerably during development and disease, requiring cardiac myocytes to be mechanically durable and capable of fusing a variety of environmental signals on different time scales. During physiological growth, myocytes adaptively remodel to mechanical loads. Pathological stimuli can induce maladaptive remodeling. In both of these conditions, the cytoskeleton plays a pivotal role in both sensing mechanical stress and mediating structural remodeling and functional responses within the myocyte.


Mechanotransduction Heart Cytoskeleton Cardiac sarcomere Cardiac myocytes Mechanosensitivity 


  1. 1.
    Adams CL, Chen YT, Smith SJ, Nelson WJ (1998) Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J Cell Biol 142:1105–1119PubMedGoogle Scholar
  2. 2.
    Ahmad F, Banerjee SK, Lage ML, Huang XN, Smith SH, Saba S, Rager J, Conner DA, Janczewski AM, Tobita K, Tinney JP, Moskowitz IP, Perez-Atayde AR, Keller BB, Mathier MA, Shroff SG, Seidman CE, Seidman JG (2008) The role of cardiac troponin T quantity and function in cardiac development and dilated cardiomyopathy. PLoS ONE 3:e2642PubMedGoogle Scholar
  3. 3.
    Aihara Y, Kurabayashi M, Saito Y, Ohyama Y, Tanaka T, Takeda S, Tomaru K, Sekiguchi K, Arai M, Nakamura T, Nagai R (2000) Cardiac ankyrin repeat protein is a novel marker of cardiac hypertrophy: role of M-CAT element within the promoter. Hypertension 36:48–53PubMedGoogle Scholar
  4. 4.
    Anastasi G, Cutroneo G, Gaeta R, Di Mauro D, Arco A, Consolo A, Santoro G, Trimarchi F, Favaloro A (2009) Dystrophin-glycoprotein complex and vinculin-talin-integrin system in human adult cardiac muscle. Int J Mol Med 23:149–159PubMedGoogle Scholar
  5. 5.
    Angst BD, Khan LU, Severs NJ, Whitely K, Rothery S, Thompson RP, Magee AI, Gourdie RG (1997) Dissociated spatial patterning of gap junctions and cell adhesion junctions during postnatal differentiation of ventricular myocardium. Circ Res 80:88–94PubMedGoogle Scholar
  6. 6.
    Anversa P, Ricci R, Olivetti G (1986) Quantitative structural analysis of the myocardium during physiologic growth and induced cardiac hypertrophy: a review. J Am Coll Cardiol 7:1140–1149PubMedGoogle Scholar
  7. 7.
    Auman HJ, Coleman H, Riley HE, Olale F, Tsai HJ, Yelon D (2007) Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol 5:e53PubMedGoogle Scholar
  8. 8.
    Babbitt CJ, Shai SY, Harpf AE, Pham CG, Ross RS (2002) Modulation of integrins and integrin signaling molecules in the pressure-loaded murine ventricle. Histochem Cell Biol 118:431–439PubMedGoogle Scholar
  9. 9.
    Bajaj P, Tang X, Saif TA, Bashir R (2010) Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes. J Biomed Mater Res A 95:1261–1269PubMedGoogle Scholar
  10. 10.
    Baker EL, Zaman MH (2010) The biomechanical integrin. J Biomech 43:38–44PubMedGoogle Scholar
  11. 11.
    Beauchamp P, Choby C, Desplantez T, de Peyer K, Green K, Yamada KA, Weingart R, Saffitz JE, Kleber AG (2004) Electrical propagation in synthetic ventricular myocyte strands from germline connexin43 knockout mice. Circ Res 95:170–178PubMedGoogle Scholar
  12. 12.
    Belkin AM, Zhidkova NI, Balzac F, Altruda F, Tomatis D, Maier A, Tarone G, Koteliansky VE, Burridge K (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 132:211–226PubMedGoogle Scholar
  13. 13.
    Beltrami CA, Finato N, Rocco M, Feruglio GA, Puricelli C, Cigola E, Sonnenblick EH, Olivetti G, Anversa P (1995) The cellular basis of dilated cardiomyopathy in humans. J Mol Cell Cardiol 27:291–305PubMedGoogle Scholar
  14. 14.
    Bendig G, Grimmler M, Huttner IG, Wessels G, Dahme T, Just S, Trano N, Katus HA, Fishman MC, Rottbauer W (2006) Integrin-linked kinase, a novel component of the cardiac mechanical stretch sensor, controls contractility in the zebrafish heart. Genes Dev 20:2361–2372PubMedGoogle Scholar
  15. 15.
    Berdougo E, Coleman H, Lee DH, Stainier DY, Yelon D (2003) Mutation of weak atrium/atrial myosin heavy chain disrupts atrial function and influences ventricular morphogenesis in zebrafish. Development 130:6121–6129PubMedGoogle Scholar
  16. 16.
    Berry MF, Engler AJ, Woo YJ, Pirolli TJ, Bish LT, Jayasankar V, Morine KJ, Gardner TJ, Discher DE, Sweeney HL (2006) Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol 290:H2196–H2203PubMedGoogle Scholar
  17. 17.
    Bhana B, Iyer RK, Chen WL, Zhao R, Sider KL, Likhitpanichkul M, Simmons CA, Radisic M (2010) Influence of substrate stiffness on the phenotype of heart cells. Biotechnol Bioeng 105:1148–1160PubMedGoogle Scholar
  18. 18.
    Bien H, Yin L, Entcheva E (2003) Cardiac cell networks on elastic microgrooved scaffolds. IEEE Eng Med Biol Mag 22:108–112PubMedGoogle Scholar
  19. 19.
    Blaauw E, van Nieuwenhoven FA, Willemsen P, Delhaas T, Prinzen FW, Snoeckx LH, van Bilsen M, van der Vusse GJ (2010) Stretch-induced hypertrophy of isolated adult rabbit cardiomyocytes. Am J Physiol Heart Circ Physiol 299:H780–H787PubMedGoogle Scholar
  20. 20.
    Boateng SY, Belin RJ, Geenen DL, Margulies KB, Martin JL, Hoshijima M, de Tombe PP, Russell B (2007) Cardiac dysfunction and heart failure are associated with abnormalities in the subcellular distribution and amounts of oligomeric muscle LIM protein. Am J Physiol Heart Circ Physiol 292:H259–H269PubMedGoogle Scholar
  21. 21.
    Boland J, Troquet J (1980) Intracellular action potential changes induced in both ventricles of the rat by an acute right ventricular pressure overload. Cardiovasc Res 14:735–740PubMedGoogle Scholar
  22. 22.
    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 2:211–218PubMedGoogle Scholar
  23. 23.
    Borg TK, Rubin K, Lundgren E, Borg K, Obrink B (1984) Recognition of extracellular matrix components by neonatal and adult cardiac myocytes. Dev Biol 104:86–96PubMedGoogle Scholar
  24. 24.
    Brancaccio M, Fratta L, Notte A, Hirsch E, Poulet R, Guazzone S, De Acetis M, Vecchione C, Marino G, Altruda F, Silengo L, Tarone G, Lembo G (2003) Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat Med 9:68–75PubMedGoogle Scholar
  25. 25.
    Brancaccio M, Guazzone S, Menini N, Sibona E, Hirsch E, De Andrea M, Rocchi M, Altruda F, Tarone G, Silengo L (1999) Melusin is a new muscle-specific interactor for beta(1) integrin cytoplasmic domain. J Biol Chem 274:29282–29288PubMedGoogle Scholar
  26. 26.
    Brancaccio M, Hirsch E, Notte A, Selvetella G, Lembo G, Tarone G (2006) Integrin signalling: the tug-of-war in heart hypertrophy. Cardiovasc Res 70:422–433PubMedGoogle Scholar
  27. 27.
    Brangwynne CP, MacKintosh FC, Kumar S, Geisse NA, Talbot J, Mahadevan L, Parker KK, Ingber DE, Weitz DA (2006) Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J Cell Biol 173:733–741PubMedGoogle Scholar
  28. 28.
    Bray MA, Sheehy SP, Parker KK (2008) Sarcomere alignment is regulated by myocyte shape. Cell Motil Cytoskeleton 65:641–651PubMedGoogle Scholar
  29. 29.
    Bullard TA, Borg TK, Price RL (2005) The expression and role of protein kinase C in neonatal cardiac myocyte attachment, cell volume, and myofibril formation is dependent on the composition of the extracellular matrix. Microsc Microanal 11:224–234PubMedGoogle Scholar
  30. 30.
    Bullard TA, Hastings JL, Davis JM, Borg TK, Price RL (2007) Altered PKC expression and phosphorylation in response to the nature, direction, and magnitude of mechanical stretch. Can J Physiol Pharmacol 85:243–250PubMedGoogle Scholar
  31. 31.
    Bursac N, Parker KK, Iravanian S, Tung L (2002) Cardiomyocyte cultures with controlled macroscopic anisotropy: a model for functional electrophysiological studies of cardiac muscle. Circ Res 91:e45–e54PubMedGoogle Scholar
  32. 32.
    Cadre BM, Qi M, Eble DM, Shannon TR, Bers DM, Samarel AM (1998) Cyclic stretch down-regulates calcium transporter gene expression in neonatal rat ventricular myocytes. J Mol Cell Cardiol 30:2247–2259PubMedGoogle Scholar
  33. 33.
    Capasso JM, Fitzpatrick D, Anversa P (1992) Cellular mechanisms of ventricular failure: myocyte kinetics and geometry with age. Am J Physiol 262:H1770–H1781PubMedGoogle Scholar
  34. 34.
    Carver W, Price RL, Raso DS, Terracio L, Borg TK (1994) Distribution of beta-1 integrin in the developing rat heart. J Histochem Cytochem 42:167–175PubMedGoogle Scholar
  35. 35.
    Carver W, Terracio L, Borg TK (1993) Expression and accumulation of interstitial collagen in the neonatal rat heart. Anat Rec 236:511–520PubMedGoogle Scholar
  36. 36.
    Chen CS, Alonso JL, Ostuni E, Whitesides GM, Ingber DE (2003) Cell shape provides global control of focal adhesion assembly. Biochem Biophys Res Commun 307:355–361PubMedGoogle Scholar
  37. 37.
    Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276:1425–1428PubMedGoogle Scholar
  38. 38.
    Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1998) Micropatterned surfaces for control of cell shape, position, and function. Biotechnol Prog 14:356–363PubMedGoogle Scholar
  39. 39.
    Choquet D, Felsenfeld DP, Sheetz MP (1997) Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88:39–48PubMedGoogle Scholar
  40. 40.
    Chung CY, Bien H, Entcheva E (2007) The role of cardiac tissue alignment in modulating electrical function. J Cardiovasc Electrophysiol 18:1323–1329PubMedGoogle Scholar
  41. 41.
    Chung CY, Bien H, Sobie EA, Dasari V, McKinnon D, Rosati B, Entcheva E (2010) Hypertrophic phenotype in cardiac cell assemblies solely by structural cues and ensuing self-organization. FASEB J (in press)Google Scholar
  42. 42.
    Clark WA, Decker ML, Behnke-Barclay M, Janes DM, Decker RS (1998) Cell contact as an independent factor modulating cardiac myocyte hypertrophy and survival in long-term primary culture. J Mol Cell Cardiol 30:139–155PubMedGoogle Scholar
  43. 43.
    Clark KL, Yutzey KE, Benson DW (2006) Transcription factors and congenital heart defects. Annu Rev Physiol 68:97–121PubMedGoogle Scholar
  44. 44.
    Danen EH, Sonneveld P, Brakebusch C, Fassler R, Sonnenberg A (2002) The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis. J Cell Biol 159:1071–1086PubMedGoogle Scholar
  45. 45.
    Danowski BA, Imanaka-Yoshida K, Sanger JM, Sanger JW (1992) Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes. J Cell Biol 118:1411–1420PubMedGoogle Scholar
  46. 46.
    de Jonge HW, Dekkers DH, Houtsmuller AB, Sharma HS, Lamers JM (2007) Differential signaling and hypertrophic responses in cyclically stretched vs endothelin-1 stimulated neonatal rat cardiomyocytes. Cell Biochem Biophys 47:21–32PubMedGoogle Scholar
  47. 47.
    de Melker AA, Sonnenberg A (1999) Integrins: alternative splicing as a mechanism to regulate ligand binding and integrin signaling events. Bioessays 21:499–509PubMedGoogle Scholar
  48. 48.
    de Pater E, Clijsters L, Marques SR, Lin YF, Garavito-Aguilar ZV, Yelon D, Bakkers J (2009) Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 136:1633–1641PubMedGoogle Scholar
  49. 49.
    de Tombe PP, Mateja RD, Tachampa K, Mou YA, Farman GP, Irving TC (2010) Myofilament length dependent activation. J Mol Cell Cardiol 48:851–858PubMedGoogle Scholar
  50. 50.
    Desai RA, Gao L, Raghavan S, Liu WF, Chen CS (2009) Cell polarity triggered by cell-cell adhesion via E-cadherin. J Cell Sci 122:905–911PubMedGoogle Scholar
  51. 51.
    Domian IJ, Chiravuri M, van der Meer P, Feinberg AW, Shi X, Shao Y, Wu SM, Parker KK, Chien KR (2009) Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 326:426–429PubMedGoogle Scholar
  52. 52.
    Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang HY, Speicher DW, Sanger JW, Sanger JM, Discher DE (2008) Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci 121:3794–3802PubMedGoogle Scholar
  53. 53.
    Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689PubMedGoogle Scholar
  54. 54.
    Entcheva E, Bien H (2005) Acoustic micromachining of three-dimensional surfaces for biological applications. Lab Chip 5:179–183PubMedGoogle Scholar
  55. 55.
    Falconnet D, Csucs G, Grandin HM, Textor M (2006) Surface engineering approaches to micropattern surfaces for cell-based assays. Biomaterials 27:3044–3063PubMedGoogle Scholar
  56. 56.
    Farhadian F, Contard F, Corbier A, Barrieux A, Rappaport L, Samuel JL (1995) Fibronectin expression during physiological and pathological cardiac growth. J Mol Cell Cardiol 27:981–990PubMedGoogle Scholar
  57. 57.
    Fassler R, Rohwedel J, Maltsev V, Bloch W, Lentini S, Guan K, Gullberg D, Hescheler J, Addicks K, Wobus AM (1996) Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin. J Cell Sci 109(Pt 13):2989–2999PubMedGoogle Scholar
  58. 58.
    Fast VG, Kleber AG (1993) Microscopic conduction in cultured strands of neonatal rat heart cells measured with voltage-sensitive dyes. Circ Res 73:914–925PubMedGoogle Scholar
  59. 59.
    Feinberg AW, Feigel A, Shevkoplyas SS, Sheehy S, Whitesides GM, Parker KK (2007) Muscular thin films for building actuators and powering devices. Science 317:1366–1370PubMedGoogle Scholar
  60. 60.
    Fishman MC, Chien KR (1997) Fashioning the vertebrate heart: earliest embryonic decisions. Development 124:2099–2117PubMedGoogle Scholar
  61. 61.
    Flick MJ, Konieczny SF (2000) The muscle regulatory and structural protein MLP is a cytoskeletal binding partner of betaI-spectrin. J Cell Sci 113(Pt 9):1553–1564PubMedGoogle Scholar
  62. 62.
    Folkman J, Moscona A (1978) Role of cell shape in growth control. Nature 273:345–349PubMedGoogle Scholar
  63. 63.
    Frank D, Kuhn C, Brors B, Hanselmann C, Ludde M, Katus HA, Frey N (2008) Gene expression pattern in biomechanically stretched cardiomyocytes: evidence for a stretch-specific gene program. Hypertension 51:309–318PubMedGoogle Scholar
  64. 64.
    Franz MR, Burkhoff D, Yue DT, Sagawa K (1989) Mechanically induced action potential changes and arrhythmia in isolated and in situ canine hearts. Cardiovasc Res 23:213–223PubMedGoogle Scholar
  65. 65.
    Franz MR, Cima R, Wang D, Profitt D, Kurz R (1992) Electrophysiological effects of myocardial stretch and mechanical determinants of stretch-activated arrhythmias. Circulation 86:968–978PubMedGoogle Scholar
  66. 66.
    Furst DO, Osborn M, Nave R, Weber K (1988) The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J Cell Biol 106:1563–1572PubMedGoogle Scholar
  67. 67.
    Furukawa T, Yamane T, Terai T, Katayama Y, Hiraoka M (1996) Functional linkage of the cardiac ATP-sensitive K+ channel to the actin cytoskeleton. Pflugers Arch 431:504–512PubMedGoogle Scholar
  68. 68.
    Galli A, DeFelice LJ (1994) Inactivation of L-type Ca channels in embryonic chick ventricle cells: dependence on the cytoskeletal agents colchicine and taxol. Biophys J 67:2296–2304PubMedGoogle Scholar
  69. 69.
    Ganz A, Lambert M, Saez A, Silberzan P, Buguin A, Mege RM, Ladoux B (2006) Traction forces exerted through N-cadherin contacts. Biol Cell 98:721–730PubMedGoogle Scholar
  70. 70.
    Gaudesius G, Miragoli M, Thomas SP, Rohr S (2003) Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ Res 93:421–428PubMedGoogle Scholar
  71. 71.
    Geiger B, Bershadsky A (2001) Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 13:584–592PubMedGoogle Scholar
  72. 72.
    Geisse NA, Sheehy SP, Parker KK (2009) Control of myocyte remodeling in vitro with engineered substrates. In Vitro Cell Dev Biol Anim 45:343–350PubMedGoogle Scholar
  73. 73.
    Gerdes AM (1992) Remodeling of ventricular myocytes during cardiac hypertrophy and heart failure. J Fla Med Assoc 79:253–255PubMedGoogle Scholar
  74. 74.
    Gerdes AM (2002) Cardiac myocyte remodeling in hypertrophy and progression to failure. J Card Fail 8:S264–S268PubMedGoogle Scholar
  75. 75.
    Gerdes AM, Capasso JM (1995) Structural remodeling and mechanical dysfunction of cardiac myocytes in heart failure. J Mol Cell Cardiol 27:849–856PubMedGoogle Scholar
  76. 76.
    Gerdes AM, Kellerman SE, Moore JA, Muffly KE, Clark LC, Reaves PY, Malec KB, McKeown PP, Schocken DD (1992) Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation 86:426–430PubMedGoogle Scholar
  77. 77.
    Goncharova EJ, Kam Z, Geiger B (1992) The involvement of adherens junction components in myofibrillogenesis in cultured cardiac myocytes. Development 114:173–183PubMedGoogle Scholar
  78. 78.
    Gopalan SM, Flaim C, Bhatia SN, Hoshijima M, Knoell R, Chien KR, Omens JH, McCulloch AD (2003) Anisotropic stretch-induced hypertrophy in neonatal ventricular myocytes micropatterned on deformable elastomers. Biotechnol Bioeng 81:578–587PubMedGoogle Scholar
  79. 79.
    Gourdie RG, Green CR, Severs NJ (1991) Gap junction distribution in adult mammalian myocardium revealed by an anti-peptide antibody and laser scanning confocal microscopy. J Cell Sci 99(Pt 1):41–55PubMedGoogle Scholar
  80. 80.
    Gourdie RG, Green CR, Severs NJ, Thompson RP (1992) Immunolabelling patterns of gap junction connexins in the developing and mature rat heart. Anat Embryol (Berl) 185:363–378Google Scholar
  81. 81.
    Grant DA (1999) Ventricular constraint in the fetus and newborn. Can J Cardiol 15:95–104PubMedGoogle Scholar
  82. 82.
    Granzier HL, Radke MH, Peng J, Westermann D, Nelson OL, Rost K, King NM, Yu Q, Tschope C, McNabb M, Larson DF, Labeit S, Gotthardt M (2009) Truncation of titin's elastic PEVK region leads to cardiomyopathy with diastolic dysfunction. Circ Res 105:557–564Google Scholar
  83. 83.
    Grossman W, Jones D, McLaurin LP (1975) Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest 56:56–64PubMedGoogle Scholar
  84. 84.
    Gwak SJ, Bhang SH, Kim IK, Kim SS, Cho SW, Jeon O, Yoo KJ, Putnam AJ, Kim BS (2008) The effect of cyclic strain on embryonic stem cell-derived cardiomyocytes. Biomaterials 29:844–856PubMedGoogle Scholar
  85. 85.
    Harris TJ, Tepass U (2010) Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11:502–514PubMedGoogle Scholar
  86. 86.
    Helmes M, Trombitas K, Centner T, Kellermayer M, Labeit S, Linke WA, Granzier H (1999) Mechanically driven contour-length adjustment in rat cardiac titin’s unique N2B sequence: titin is an adjustable spring. Circ Res 84:1339–1352PubMedGoogle Scholar
  87. 87.
    Helmes M, Trombitas K, Granzier H (1996) Titin develops restoring force in rat cardiac myocytes. Circ Res 79:619–626PubMedGoogle Scholar
  88. 88.
    Hertig CM, Eppenberger-Eberhardt M, Koch S, Eppenberger HM (1996) N-cadherin in adult rat cardiomyocytes in culture. I. Functional role of N-cadherin and impairment of cell-cell contact by a truncated N-cadherin mutant. J Cell Sci 109(Pt 1):1–10PubMedGoogle Scholar
  89. 89.
    Hilenski LL, Ma XH, Vinson N, Terracio L, Borg TK (1992) The role of beta 1 integrin in spreading and myofibrillogenesis in neonatal rat cardiomyocytes in vitro. Cell Motil Cytoskeleton 21:87–100PubMedGoogle Scholar
  90. 90.
    Hilenski LL, Terracio L, Borg TK (1991) Myofibrillar and cytoskeletal assembly in neonatal rat cardiac myocytes cultured on laminin and collagen. Cell Tissue Res 264:577–587PubMedGoogle Scholar
  91. 91.
    Hilenski LL, Terracio L, Sawyer R, Borg TK (1989) Effects of extracellular matrix on cytoskeletal and myofibrillar organization in vitro. Scanning Microsc 3:535–548PubMedGoogle Scholar
  92. 92.
    Hirschy A, Schatzmann F, Ehler E, Perriard JC (2006) Establishment of cardiac cytoarchitecture in the developing mouse heart. Dev Biol 289:430–441PubMedGoogle Scholar
  93. 93.
    Hornberger LK, Singhroy S, Cavalle-Garrido T, Tsang W, Keeley F, Rabinovitch M (2000) Synthesis of extracellular matrix and adhesion through beta(1) integrins are critical for fetal ventricular myocyte proliferation. Circ Res 87:508–515PubMedGoogle Scholar
  94. 94.
    Hoshijima M (2006) Mechanical stress-strain sensors embedded in cardiac cytoskeleton: Z disk, titin, and associated structures. Am J Physiol Heart Circ Physiol 290:H1313–H1325PubMedGoogle Scholar
  95. 95.
    Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172–177PubMedGoogle Scholar
  96. 96.
    Humphries MJ (2000) Integrin structure. Biochem Soc Trans 28:311–339PubMedGoogle Scholar
  97. 97.
    Humphries JD, Byron A, Humphries MJ (2006) Integrin ligands at a glance. J Cell Sci 119:3901–3903PubMedGoogle Scholar
  98. 98.
    Icardo JM, Ojeda JL (1984) Effects of colchicine on the formation and looping of the tubular heart of the embryonic chick. Acta Anat (Basel) 119:1–9Google Scholar
  99. 99.
    Imanaka-Yoshida K, Knudsen KA, Linask KK (1998) N-cadherin is required for the differentiation and initial myofibrillogenesis of chick cardiomyocytes. Cell Motil Cytoskeleton 39:52–62PubMedGoogle Scholar
  100. 100.
    Ingber DE (2003) Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci 116:1157–1173PubMedGoogle Scholar
  101. 101.
    Ingber DE (2006) Cellular mechanotransduction: putting all the pieces together again. FASEB J 20:811–827PubMedGoogle Scholar
  102. 102.
    Itasaki N, Nakamura H, Sumida H, Yasuda M (1991) Actin bundles on the right side in the caudal part of the heart tube play a role in dextro-looping in the embryonic chick heart. Anat Embryol (Berl) 183:29–39Google Scholar
  103. 103.
    Jacot JG, McCulloch AD, Omens JH (2008) Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 95:3479–3487PubMedGoogle Scholar
  104. 104.
    Kamisago M, Sharma SD, DePalma SR, Solomon S, Sharma P, McDonough B, Smoot L, Mullen MP, Woolf PK, Wigle ED, Seidman JG, Seidman CE (2000) Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N Engl J Med 343:1688–1696PubMedGoogle Scholar
  105. 105.
    Katz AM (2002) Maladaptive growth in the failing heart: the cardiomyopathy of overload. Cardiovasc Drugs Ther 16:245–249PubMedGoogle Scholar
  106. 106.
    Kim DH, Lipke EA, Kim P, Cheong R, Thompson S, Delannoy M, Suh KY, Tung L, Levchenko A (2010) Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc Natl Acad Sci USA 107:565–570PubMedGoogle Scholar
  107. 107.
    Kleber AG, Rudy Y (2004) Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 84:431–488PubMedGoogle Scholar
  108. 108.
    Knoll R, Hoshijima M, Hoffman HM, Person V, Lorenzen-Schmidt I, Bang ML, Hayashi T, Shiga N, Yasukawa H, Schaper W, McKenna W, Yokoyama M, Schork NJ, Omens JH, McCulloch AD, Kimura A, Gregorio CC, Poller W, Schaper J, Schultheiss HP, Chien KR (2002) The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell 111:943–955PubMedGoogle Scholar
  109. 109.
    Kruger M, Linke WA (2009) Titin-based mechanical signalling in normal and failing myocardium. J Mol Cell Cardiol 46:490–498PubMedGoogle Scholar
  110. 110.
    Lange S, Auerbach D, McLoughlin P, Perriard E, Schafer BW, Perriard JC, Ehler E (2002) Subcellular targeting of metabolic enzymes to titin in heart muscle may be mediated by DRAL/FHL-2. J Cell Sci 115:4925–4936Google Scholar
  111. 111.
    Lapidos KA, Kakkar R, McNally EM (2004) The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 94:1023–1031PubMedGoogle Scholar
  112. 112.
    Latacha KS, Remond MC, Ramasubramanian A, Chen AY, Elson EL, Taber LA (2005) Role of actin polymerization in bending of the early heart tube. Dev Dyn 233:1272–1286PubMedGoogle Scholar
  113. 113.
    le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, de Rooij J (2010) Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol 189:1107–1115PubMedGoogle Scholar
  114. 114.
    Lele TP, Kumar S (2007) Brushes, cables, and anchors: recent insights into multiscale assembly and mechanics of cellular structural networks. Cell Biochem Biophys 47:348–360PubMedGoogle Scholar
  115. 115.
    LeWinter MM, Granzier H (2010) Cardiac titin: a multifunctional giant. Circulation 121:2137–2145PubMedGoogle Scholar
  116. 116.
    Linke WA (2008) Sense and stretchability: the role of titin and titin-associated proteins in myocardial stress-sensing and mechanical dysfunction. Cardiovasc Res 77:637–648PubMedGoogle Scholar
  117. 117.
    Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ, Ruiz SA, Nelson CM, Chen CS (2010) Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci USA 107:9944–9949PubMedGoogle Scholar
  118. 118.
    Luk A, Ahn E, Soor GS, Butany J (2009) Dilated cardiomyopathy: a review. J Clin Pathol 62:219–225PubMedGoogle Scholar
  119. 119.
    Lundgren E, Terracio L, Borg TK (1985) Adhesion of cardiac myocytes to extracellular matrix components. Basic Res Cardiol 80(Suppl 1):69–74PubMedGoogle Scholar
  120. 120.
    Lundgren E, Terracio L, Mardh S, Borg TK (1985) Extracellular matrix components influence the survival of adult cardiac myocytes in vitro. Exp Cell Res 158:371–381PubMedGoogle Scholar
  121. 121.
    Luo Y, Radice GL (2003) Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus. J Cell Sci 116:1471–1479PubMedGoogle Scholar
  122. 122.
    Manasek FJ, Burnside MB, Waterman RE (1972) Myocardial cell shape change as a mechanism of embryonic heart looping. Dev Biol 29:349–371PubMedGoogle Scholar
  123. 123.
    Manasek FJ, Monroe RG (1972) Early cardiac morphogenesis is independent of function. Dev Biol 27:584–588PubMedGoogle Scholar
  124. 124.
    Manning A, McLachlan JC (1990) Looping of chick embryo hearts in vitro. J Anat 168:257–263PubMedGoogle Scholar
  125. 125.
    Matthews BD, Overby DR, Mannix R, Ingber DE (2006) Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 119:508–518PubMedGoogle Scholar
  126. 126.
    Meyer CJ, Alenghat FJ, Rim P, Fong JH, Fabry B, Ingber DE (2000) Mechanical control of cyclic AMP signalling and gene transcription through integrins. Nat Cell Biol 2:666–668PubMedGoogle Scholar
  127. 127.
    Miller MK, Bang ML, Witt CC, Labeit D, Trombitas C, Watanabe K, Granzier H, McElhinny AS, Gregorio CC, Labeit S (2003) The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules. J Mol Biol 333:951–964PubMedGoogle Scholar
  128. 128.
    Moorman AF, Christoffels VM (2003) Cardiac chamber formation: development, genes, and evolution. Physiol Rev 83:1223–1267PubMedGoogle Scholar
  129. 129.
    Mrksich M, Chen CS, Xia Y, Dike LE, Ingber DE, Whitesides GM (1996) Controlling cell attachment on contoured surfaces with self-assembled monolayers of alkanethiolates on gold. Proc Natl Acad Sci USA 93:10775–10778PubMedGoogle Scholar
  130. 130.
    Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S, Witt CC, Becker K, Labeit S, Granzier HL (2004) Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110:155–162PubMedGoogle Scholar
  131. 131.
    Nawata J, Ohno I, Isoyama S, Suzuki J, Miura S, Ikeda J, Shirato K (1999) Differential expression of alpha 1, alpha 3 and alpha 5 integrin subunits in acute and chronic stages of myocardial infarction in rats. Cardiovasc Res 43:371–381PubMedGoogle Scholar
  132. 132.
    Niimura H, Patton KK, McKenna WJ, Soults J, Maron BJ, Seidman JG, Seidman CE (2002) Sarcomere protein gene mutations in hypertrophic cardiomyopathy of the elderly. Circulation 105:446–451PubMedGoogle Scholar
  133. 133.
    Olivetti G, Ricci R, Lagrasta C, Maniga E, Sonnenblick EH, Anversa P (1988) Cellular basis of wall remodeling in long-term pressure overload-induced right ventricular hypertrophy in rats. Circ Res 63:648–657PubMedGoogle Scholar
  134. 134.
    Oliviero P, Chassagne C, Salichon N, Corbier A, Hamon G, Marotte F, Charlemagne D, Rappaport L, Samuel JL (2000) Expression of laminin alpha2 chain during normal and pathological growth of myocardium in rat and human. Cardiovasc Res 46:346–355PubMedGoogle Scholar
  135. 135.
    Parker KK, Brock AL, Brangwynne C, Mannix RJ, Wang N, Ostuni E, Geisse NA, Adams JC, Whitesides GM, Ingber DE (2002) Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces. FASEB J 16:1195–1204PubMedGoogle Scholar
  136. 136.
    Parker KK, Ingber DE (2007) Extracellular matrix, mechanotransduction and structural hierarchies in heart tissue engineering. Philos Trans R Soc Lond B Biol Sci 362:1267–1279PubMedGoogle Scholar
  137. 137.
    Parker KK, Tan J, Chen CS, Tung L (2008) Myofibrillar architecture in engineered cardiac myocytes. Circ Res 103:340–342PubMedGoogle Scholar
  138. 138.
    Parker KK, Taylor LK, Atkinson JB, Hansen DE, Wikswo JP (2001) The effects of tubulin-binding agents on stretch-induced ventricular arrhythmias. Eur J Pharmacol 417:131–140PubMedGoogle Scholar
  139. 139.
    Pedrotty DM, Klinger RY, Badie N, Hinds S, Kardashian A, Bursac N (2008) Structural coupling of cardiomyocytes and noncardiomyocytes: quantitative comparisons using a novel micropatterned cell pair assay. Am J Physiol Heart Circ Physiol 295:H390–H400PubMedGoogle Scholar
  140. 140.
    Pelham RJ Jr, Wang Y (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94:13661–13665PubMedGoogle Scholar
  141. 141.
    Peters NS, Severs NJ, Rothery SM, Lincoln C, Yacoub MH, Green CR (1994) Spatiotemporal relation between gap junctions and fascia adherens junctions during postnatal development of human ventricular myocardium. Circulation 90:713–725PubMedGoogle Scholar
  142. 142.
    Pham CG, Harpf AE, Keller RS, Vu HT, Shai SY, Loftus JC, Ross RS (2000) Striated muscle-specific beta(1D)-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am J Physiol Heart Circ Physiol 279:H2916–H2926PubMedGoogle Scholar
  143. 143.
    Pijnappels DA, Schalij MJ, Ramkisoensing AA, van Tuyn J, de Vries AA, van der Laarse A, Ypey DL, Atsma DE (2008) Forced alignment of mesenchymal stem cells undergoing cardiomyogenic differentiation affects functional integration with cardiomyocyte cultures. Circ Res 103:167–176PubMedGoogle Scholar
  144. 144.
    Price RL, Chintanowonges C, Shiraishi I, Borg TK, Terracio L (1996) Local and regional variations in myofibrillar patterns in looping rat hearts. Anat Rec 245:83–93PubMedGoogle Scholar
  145. 145.
    Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO (1997) Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181:64–78PubMedGoogle Scholar
  146. 146.
    Remond MC, Fee JA, Elson EL, Taber LA (2006) Myosin-based contraction is not necessary for cardiac c-looping in the chick embryo. Anat Embryol (Berl) 211:443–454Google Scholar
  147. 147.
    Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302:1704–1709PubMedGoogle Scholar
  148. 148.
    Ross RS, Borg TK (2001) Integrins and the myocardium. Circ Res 88:1112–1119PubMedGoogle Scholar
  149. 149.
    Ross RS, Pham C, Shai SY, Goldhaber JI, Fenczik C, Glembotski CC, Ginsberg MH, Loftus JC (1998) Beta1 integrins participate in the hypertrophic response of rat ventricular myocytes. Circ Res 82:1160–1172PubMedGoogle Scholar
  150. 150.
    Salameh A, Wustmann A, Karl S, Blanke K, Apel D, Rojas-Gomez D, Franke H, Mohr FW, Janousek J, Dhein S (2010) Cyclic mechanical stretch induces cardiomyocyte orientation and polarization of the gap junction protein connexin43. Circ Res 106:1592–1602PubMedGoogle Scholar
  151. 151.
    Samuel JL, Barrieux A, Dufour S, Dubus I, Contard F, Koteliansky V, Farhadian F, Marotte F, Thiery JP, Rappaport L (1991) Accumulation of fetal fibronectin mRNAs during the development of rat cardiac hypertrophy induced by pressure overload. J Clin Invest 88:1737–1746PubMedGoogle Scholar
  152. 152.
    Samuel JL, Farhadian F, Sabri A, Marotte F, Robert V, Rappaport L (1994) Expression of fibronectin during rat fetal and postnatal development: an in situ hybridisation and immunohistochemical study. Cardiovasc Res 28:1653–1661PubMedGoogle Scholar
  153. 153.
    Schaper J, Speiser B (1992) The extracellular matrix in the failing human heart. Basic Res Cardiol 87(Suppl 1):303–309PubMedGoogle Scholar
  154. 154.
    Schwartz MA, Ginsberg MH (2002) Networks and crosstalk: integrin signalling spreads. Nat Cell Biol 4:E65–E68PubMedGoogle Scholar
  155. 155.
    Sheikh F, Raskin A, Chu PH, Lange S, Domenighetti AA, Zheng M, Liang X, Zhang T, Yajima T, Gu Y, Dalton ND, Mahata SK, Dorn GW, 2nd, Heller-Brown J, Peterson KL, Omens JH, McCulloch AD, Chen J (2008) An FHL1-containing complex within the cardiomyocyte sarcomere mediates hypertrophic biomechanical stress responses in mice. J Clin Invest 118:3870–3880Google Scholar
  156. 156.
    Shimko VF, Claycomb WC (2008) Effect of mechanical loading on three-dimensional cultures of embryonic stem cell-derived cardiomyocytes. Tissue Eng A 14:49–58Google Scholar
  157. 157.
    Simpson DG, Decker ML, Clark WA, Decker RS (1993) Contractile activity and cell-cell contact regulate myofibrillar organization in cultured cardiac myocytes. J Cell Biol 123:323–336PubMedGoogle Scholar
  158. 158.
    Simpson DG, Majeski M, Borg TK, Terracio L (1999) Regulation of cardiac myocyte protein turnover and myofibrillar structure in vitro by specific directions of stretch. Circ Res 85:e59–e69PubMedGoogle Scholar
  159. 159.
    Simpson DG, Terracio L, Terracio M, Price RL, Turner DC, Borg TK (1994) Modulation of cardiac myocyte phenotype in vitro by the composition and orientation of the extracellular matrix. J Cell Physiol 161:89–105PubMedGoogle Scholar
  160. 160.
    Smith SH, Bishop SP (1985) Regional myocyte size in compensated right ventricular hypertrophy in the ferret. J Mol Cell Cardiol 17:1005–1011PubMedGoogle Scholar
  161. 161.
    Soler AP, Knudsen KA (1994) N-cadherin involvement in cardiac myocyte interaction and myofibrillogenesis. Dev Biol 162:9–17PubMedGoogle Scholar
  162. 162.
    Soufan AT, van den Berg G, Ruijter JM, de Boer PA, van den Hoff MJ, Moorman AF (2006) Regionalized sequence of myocardial cell growth and proliferation characterizes early chamber formation. Circ Res 99:545–552PubMedGoogle Scholar
  163. 163.
    Spach MS, Heidlage JF, Barr RC, Dolber PC (2004) Cell size and communication: role in structural and electrical development and remodeling of the heart. Heart Rhythm 1:500–515PubMedGoogle Scholar
  164. 164.
    Spach MS, Heidlage JF, Dolber PC, Barr RC (2000) Electrophysiological effects of remodeling cardiac gap junctions and cell size: experimental and model studies of normal cardiac growth. Circ Res 86:302–311PubMedGoogle Scholar
  165. 165.
    Srivastava D, Olson EN (2000) A genetic blueprint for cardiac development. Nature 407:221–226PubMedGoogle Scholar
  166. 166.
    Taber LA (2001) Biomechanics of cardiovascular development. Annu Rev Biomed Eng 3:1–25PubMedGoogle Scholar
  167. 167.
    Taber LA, Lin IE, Clark EB (1995) Mechanics of cardiac looping. Dev Dyn 203:42–50PubMedGoogle Scholar
  168. 168.
    Tagawa H, Wang N, Narishige T, Ingber DE, Zile MR, Cooper Gt (1997) Cytoskeletal mechanics in pressure-overload cardiac hypertrophy. Circ Res 80:281–289PubMedGoogle Scholar
  169. 169.
    Tay CY, Yu H, Pal M, Leong WS, Tan NS, Ng KW, Leong DT, Tan LP (2010) Micropatterned matrix directs differentiation of human mesenchymal stem cells towards myocardial lineage. Exp Cell Res 316:1159–1168PubMedGoogle Scholar
  170. 170.
    Terracio L, Rubin K, Gullberg D, Balog E, Carver W, Jyring R, Borg TK (1991) Expression of collagen binding integrins during cardiac development and hypertrophy. Circ Res 68:734–744PubMedGoogle Scholar
  171. 171.
    Terzic A, Kurachi Y (1996) Actin microfilament disrupters enhance K(ATP) channel opening in patches from guinea-pig cardiomyocytes. J Physiol 492(Pt 2):395–404PubMedGoogle Scholar
  172. 172.
    Thomas SP, Kucera JP, Bircher-Lehmann L, Rudy Y, Saffitz JE, Kleber AG (2003) Impulse propagation in synthetic strands of neonatal cardiac myocytes with genetically reduced levels of connexin43. Circ Res 92:1209–1216PubMedGoogle Scholar
  173. 173.
    Tobita K, Schroder EA, Tinney JP, Garrison JB, Keller BB (2002) Regional passive ventricular stress-strain relations during development of altered loads in chick embryo. Am J Physiol Heart Circ Physiol 282:H2386–H2396PubMedGoogle Scholar
  174. 174.
    Torsoni AS, Constancio SS, Nadruz W Jr, Hanks SK, Franchini KG (2003) Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes. Circ Res 93:140–147PubMedGoogle Scholar
  175. 175.
    Tsutsui H, Ishihara K, Gt C (1993) Cytoskeletal role in the contractile dysfunction of hypertrophied myocardium. Science 260:682–687PubMedGoogle Scholar
  176. 176.
    Tsutsui H, Tagawa H, Kent RL, McCollam PL, Ishihara K, Nagatsu M, Gt C (1994) Role of microtubules in contractile dysfunction of hypertrophied cardiocytes. Circulation 90:533–555PubMedGoogle Scholar
  177. 177.
    Ulrich MM, Janssen AM, Daemen MJ, Rappaport L, Samuel JL, Contard F, Smits JF, Cleutjens JP (1997) Increased expression of fibronectin isoforms after myocardial infarction in rats. J Mol Cell Cardiol 29:2533–2543PubMedGoogle Scholar
  178. 178.
    van den Berg G, Abu-Issa R, de Boer BA, Hutson MR, de Boer PA, Soufan AT, Ruijter JM, Kirby ML, van den Hoff MJ, Moorman AF (2009) A caudal proliferating growth center contributes to both poles of the forming heart tube. Circ Res 104:179–188PubMedGoogle Scholar
  179. 179.
    van der Flier A, Gaspar AC, Thorsteinsdottir S, Baudoin C, Groeneveld E, Mummery CL, Sonnenberg A (1997) Spatial and temporal expression of the beta1D integrin during mouse development. Dev Dyn 210:472–486PubMedGoogle Scholar
  180. 180.
    Wagner M, Siddiqui MA (2007) Signal transduction in early heart development (I): cardiogenic induction and heart tube formation. Exp Biol Med (Maywood) 232:852–865Google Scholar
  181. 181.
    Walsh KB, Parks GE (2002) Changes in cardiac myocyte morphology alter the properties of voltage-gated ion channels. Cardiovasc Res 55:64–75PubMedGoogle Scholar
  182. 182.
    Werchan PM, Summer WR, Gerdes AM, McDonough KH (1989) Right ventricular performance after monocrotaline-induced pulmonary hypertension. Am J Physiol 256:H1328–H1336PubMedGoogle Scholar
  183. 183.
    White DP, Caswell PT, Norman JC (2007) alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J Cell Biol 177:515–525PubMedGoogle Scholar
  184. 184.
    Wu JC, Chung TH, Tseng YZ, Wang SM (1999) N-cadherin/catenin-based costameres in cultured chicken cardiomyocytes. J Cell Biochem 75:93–104PubMedGoogle Scholar
  185. 185.
    Wu JC, Sung HC, Chung TH, DePhilip RM (2002) Role of N-cadherin- and integrin-based costameres in the development of rat cardiomyocytes. J Cell Biochem 84:717–724PubMedGoogle Scholar
  186. 186.
    Yamada S, Nelson WJ (2007) Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J Cell Biol 178:517–527PubMedGoogle Scholar
  187. 187.
    Yin L, Bien H, Entcheva E (2004) Scaffold topography alters intracellular calcium dynamics in cultured cardiomyocyte networks. Am J Physiol Heart Circ Physiol 287:H1276–H1285PubMedGoogle Scholar
  188. 188.
    Zhuang J, Yamada KA, Saffitz JE, Kleber AG (2000) Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ Res 87:316–322PubMedGoogle Scholar
  189. 189.
    Zierhut W, Zimmer HG, Gerdes AM (1991) Effect of angiotensin converting enzyme inhibition on pressure-induced left ventricular hypertrophy in rats. Circ Res 69:609–617PubMedGoogle Scholar
  190. 190.
    Zuppinger C, Schaub MC, Eppenberger HM (2000) Dynamics of early contact formation in cultured adult rat cardiomyocytes studied by N-cadherin fused to green fluorescent protein. J Mol Cell Cardiol 32:539–555PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Disease Biophysics Group, Wyss Institute for Biologically Inspired EngineeringHarvard UniversityCambridgeUSA
  2. 2.School of Engineering and Applied SciencesHarvard UniversityCambridgeUSA

Personalised recommendations