Intercellular and extracellular mechanotransduction in cardiac myocytes

Pflugers Archiv European Journal of Physiology

Volumn 462, Issue 1, 2011, Pages 75-87

  Kresh, J Yasha ^a   Chopra, Anant ^b  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b DREXEL UNIVERSITY   (United States)

Author keywords

Cardiomyopathy; Cytoskeletal remodeling; Mechanobiology; Mechanosensing; Microenvironment; Sarcomere

Indexed keywords

ALPHA ACTININ; CATENIN; INTEGRIN; NERVE CELL ADHESION MOLECULE; VINCULIN;

ANISOTROPY; CELL ADHESION; CELL SPREADING; CELL STRESS; CONGENITAL HEART MALFORMATION; CYTOSKELETON; DIASTOLE; EXTRACELLULAR MATRIX; HEART AFTERLOAD; HEART CONTRACTION; HEART DEVELOPMENT; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE COMPLIANCE; HEART PRELOAD; HUMAN; INTERCELLULAR SPACE; MECHANOTRANSDUCTION; MICROENVIRONMENT; MUSCLE FIBRIL; MUSCLE STRETCHING; MYOFIBROBLAST; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REVIEW; SARCOMERE;

ANIMALS; CADHERINS; CELL ADHESION; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBRONECTINS; INTEGRINS; MECHANOTRANSDUCTION, CELLULAR; MODELS, ANATOMIC; MYOCYTES, CARDIAC; MYOFIBRILS; STRESS, MECHANICAL;

EID: 79958828808     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-011-0954-1     Document Type: Review

References (78)

1. H Aberle S Butz J Stappert H Weissig R Kemler H Hoschuetzky 1994 Assembly of the cadherin-catenin complex in vitro with recombinant proteins J Cell Sci 107 Pt 12 3655 3663 7706414 1:CAS:528:DyaK2MXivFyrtb0%3D
2. CL Adams WJ Nelson 1998 Cytomechanics of cadherin-mediated cell-cell adhesion Curr Opin Cell Biol 10 572 577 9818166 10.1016/S0955-0674(98)80031-8 1:CAS:528:DyaK1cXntVSgurs%3D (Pubitemid 28477014)
3. C Bierkamp KJ McLaughlin H Schwarz O Huber R Kemler 1996 Embryonic heart and skin defects in mice lacking plakoglobin Dev Biol 180 780 785 8954745 10.1006/dbio.1996.0346 1:CAS:528:DyaK2sXmslGi (Pubitemid 27037381)
4. T Brade J Manner M Kuhl 2006 The role of Wnt signalling in cardiac development and tissue remodelling in the mature heart Cardiovasc Res 72 198 209 16860783 10.1016/j.cardiores.2006.06.025 1:CAS:528:DC%2BD28XhtVygsLjM (Pubitemid 44511910)
5. M Brancaccio E Hirsch A Notte G Selvetella G Lembo G Tarone 2006 Integrin signalling: the tug-of-war in heart hypertrophy Cardiovasc Res 70 422 433 16466704 10.1016/j.cardiores.2005.12.015 1:CAS:528:DC%2BD28Xks1Wlur8%3D
6. MA Bray SP Sheehy KK Parker 2008 Sarcomere alignment is regulated by myocyte shape Cell Motil Cytoskeleton 65 641 651 18561184 10.1002/cm.20290
7. W Carver L Terracio TK Borg 1993 Expression and accumulation of interstitial collagen in the neonatal rat heart Anat Rec 236 511 520 8363055 10.1002/ar.1092360311 1:CAS:528:DyaK3sXkvFajtbk%3D (Pubitemid 23193319)
8. S Charrasse M Meriane F Comunale A Blangy C Gauthier-Rouviere 2002 N-cadherin-dependent cell-cell contact regulates Rho GTPases and beta-catenin localization in mouse C2C12 myoblasts J Cell Biol 158 953 965 12213839 10.1083/jcb.200202034 1:CAS:528:DC%2BD38XmvV2gs7o%3D (Pubitemid 35001085)
9. Chopra A, Tabdanov E, Patel H, Janmey P, Kresh JY (2011) Cardiac myocyte remodeling mediated by N-cadherin-dependent mechanosensing. Am J Physiol Heart Circ Physiol (in press)
10. D Choquet DP Felsenfeld MP Sheetz 1997 Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages Cell 88 39 48 9019403 10.1016/S0092-8674(00)81856-5 1:CAS:528:DyaK2sXltFOguw%3D%3D (Pubitemid 27180329)
11. YS Chu WA Thomas O Eder F Pincet E Perez JP Thiery S Dufour 2004 Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42 J Cell Biol 167 1183 1194 15596540 10.1083/jcb.200403043 1:CAS:528:DC%2BD2MXmsVWi (Pubitemid 40066632)
12. Cohn J, Anand I (2006) Overview: cardiac remodeling and its relationship to the development of heart failure. In: Greenberg B (ed) Cardiac remodeling: mechanisms and treatment. Taylor and Francis, New York, pp 1-8
13. VS Deshpande RM McMeeking AG Evans 2006 A bio-chemo-mechanical model for cell contractility Proc Natl Acad Sci USA 103 14015 14020 16959880 10.1073/pnas.0605837103 1:CAS:528:DC%2BD28XhtVCqs7vE (Pubitemid 44452972)
14. BJ Dzamba KR Jakab M Marsden MA Schwartz DW DeSimone 2009 Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization Dev Cell 16 421 432 19289087 10.1016/j.devcel.2009.01.008 1:CAS:528:DC%2BD1MXjs1ynsro%3D
15. AJ Engler C Carag-Krieger CP Johnson M Raab HY Tang DW Speicher JW Sanger JM Sanger DE Discher 2008 Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating J Cell Sci 121 3794 3802 18957515 10.1242/jcs.029678 1:CAS:528:DC%2BD1cXhsFaktLjO
16. AJ Engler MA Griffin S Sen CG Bonnemann HL Sweeney DE Discher 2004 Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments J Cell Biol 166 877 887 15364962 10.1083/jcb.200405004 1:CAS:528:DC%2BD2cXns1yhtb4%3D (Pubitemid 39249838)
17. AJ Engler S Sen HL Sweeney DE Discher 2006 Matrix elasticity directs stem cell lineage specification Cell 126 677 689 16923388 10.1016/j.cell.2006.06.044 1:CAS:528:DC%2BD28Xpt1aktbg%3D (Pubitemid 44233625)
18. GM Fomovsky S Thomopoulos JW Holmes 2010 Contribution of extracellular matrix to the mechanical properties of the heart J Mol Cell Cardiol 48 490 496 19686759 10.1016/j.yjmcc.2009.08.003 1:CAS:528:DC%2BC3cXitVeju7w%3D
19. JC Friedland MH Lee D Boettiger 2009 Mechanically activated integrin switch controls alpha5beta1 function Science 323 642 644 19179533 10.1126/science.1168441 1:CAS:528:DC%2BD1MXhtVOgu7Y%3D
20. A Ganz M Lambert A Saez P Silberzan A Buguin RM Mege B Ladoux 2006 Traction forces exerted through N-cadherin contacts Biol Cell 98 721 730 16895521 10.1042/BC20060039 1:CAS:528:DC%2BD28Xht1Wqur7O (Pubitemid 44896108)
21. J Gavard M Lambert I Grosheva V Marthiens T Irinopoulou JF Riou A Bershadsky RM Mege 2004 Lamellipodium extension and cadherin adhesion: two cell responses to cadherin activation relying on distinct signalling pathways J Cell Sci 117 257 270 14657280 10.1242/jcs.00857 1:CAS:528:DC%2BD2cXhtVamsLk%3D (Pubitemid 38128904)
22. J Gavard V Marthiens C Monnet M Lambert RM Mege 2004 N-cadherin activation substitutes for the cell contact control in cell cycle arrest and myogenic differentiation: involvement of p120 and beta-catenin J Biol Chem 279 36795 36802 15194693 10.1074/jbc.M401705200 1:CAS:528:DC%2BD2cXmvFCmsbo%3D (Pubitemid 39129028)
23. AM Gerdes JM Capasso 1995 Structural remodeling and mechanical dysfunction of cardiac myocytes in heart failure J Mol Cell Cardiol 27 849 856 7602601 10.1016/0022-2828(95)90000-4 1:CAS:528:DyaK2MXltVertbk%3D
24. AM Gerdes SE Kellerman JA Moore KE Muffly LC Clark PY Reaves KB Malec PP McKeown DD Schocken 1992 Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy Circulation 86 426 430 1638711 1:STN:280: DyaK38zks1yiuw%3D%3D
25. EJ Goncharova Z Kam B Geiger 1992 The involvement of adherens junction components in myofibrillogenesis in cultured cardiac myocytes Development 114 173 183 1576958 1:STN:280:DyaK383kvFajsg%3D%3D
26. MA Griffin S Sen HL Sweeney DE Discher 2004 Adhesion-contractile balance in myocyte differentiation J Cell Sci 117 5855 5863 15522893 10.1242/jcs.01496 1:CAS:528:DC%2BD2MXlvFSgug%3D%3D (Pubitemid 40136468)
27. C Hahn MA Schwartz 2009 Mechanotransduction in vascular physiology and atherogenesis Nat Rev Mol Cell Biol 10 53 62 19197332 10.1038/nrm2596 1:CAS:528:DC%2BD1MXpt1Gl
28. LL Hilenski XH Ma N Vinson L Terracio TK Borg 1992 The role of beta 1 integrin in spreading and myofibrillogenesis in neonatal rat cardiomyocytes in vitro Cell Motil Cytoskeleton 21 87 100 1373110 10.1002/cm.970210202 1:STN:280:DyaK383hslSksQ%3D%3D
29. JG Jacot JC Martin DL Hunt 2010 Mechanobiology of cardiomyocyte development J Biomech 43 93 98 19819458 10.1016/j.jbiomech.2009.09.014
30. JG Jacot AD McCulloch JH Omens 2008 Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes Biophys J 95 3479 3487 18586852 10.1529/biophysj.107.124545 1:CAS:528:DC%2BD1cXht1SrsL7O
31. TS Jou DB Stewart J Stappert WJ Nelson JA Marrs 1995 Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex Proc Natl Acad Sci USA 92 5067 5071 7761449 10.1073/pnas.92.11.5067 1:CAS:528:DyaK2MXlvFyitLo%3D
32. RS Keller SY Shai CJ Babbitt CG Pham RJ Solaro ML Valencik JC Loftus RS Ross 2001 Disruption of integrin function in the murine myocardium leads to perinatal lethality, fibrosis, and abnormal cardiac performance Am J Pathol 158 1079 1090 11238056 10.1016/S0002-9440(10)64055-2 1:CAS:528:DC%2BD3MXitlOmsrk%3D (Pubitemid 32221800)
33. I Kostetskii J Li Y Xiong R Zhou VA Ferrari VV Patel JD Molkentin GL Radice 2005 Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure Circ Res 96 346 354 15662031 10.1161/01.RES.0000156274.72390.2c 1:CAS:528:DC%2BD2MXhtF2nsb4%3D (Pubitemid 40279909)
34. EM Kovacs RG Ali AJ McCormack AS Yap 2002 E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts J Biol Chem 277 6708 6718 11744701 10.1074/jbc.M109640200 1:CAS:528:DC%2BD38XhvFyqtrg%3D (Pubitemid 34968474)
35. JY Kresh 2006 Cell replacement therapy: the functional importance of myocardial architecture and intercellular gap-junction distribution J Thorac Cardiovasc Surg 131 1310 1313 16733163 10.1016/j.jtcvs.2006.02.018 (Pubitemid 44218722)
36. M Krieg Y Arboleda-Estudillo PH Puech J Kafer F Graner DJ Muller CP Heisenberg 2008 Tensile forces govern germ-layer organization in zebrafish Nat Cell Biol 10 429 436 18364700 10.1038/ncb1705 1:CAS:528:DC%2BD1cXktVGqsbg%3D
37. M Lambert F Padilla RM Mege 2000 Immobilized dimers of N-cadherin-Fc chimera mimic cadherin-mediated cell contact formation: contribution of both outside-in and inside-out signals J Cell Sci 113 Pt 12 2207 2219 10825293 1:CAS:528:DC%2BD3cXltVGgu78%3D (Pubitemid 30426835)
38. L Larue A Bellacosa 2005 Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3' kinase/AKT pathways Oncogene 24 7443 7454 16288291 10.1038/sj.onc.1209091 1:CAS:528:DC%2BD2MXht1Wis7vE (Pubitemid 41637984)
39. J Li VV Patel I Kostetskii Y Xiong AF Chu JT Jacobson C Yu GE Morley JD Molkentin GL Radice 2005 Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis Circ Res 97 474 481 16100040 10.1161/01.RES.0000181132.11393.18 1:CAS:528:DC%2BD2MXpsVWrur4%3D (Pubitemid 41298178)
40. Z Liu JL Tan DM Cohen MT Yang NJ Sniadecki SA Ruiz CM Nelson CS Chen 2010 Mechanical tugging force regulates the size of cell-cell junctions Proc Natl Acad Sci USA 107 9944 9949 20463286 10.1073/pnas.0914547107 1:CAS:528: DC%2BC3cXnslCrsbo%3D
41. CM Lo HB Wang M Dembo YL Wang 2000 Cell movement is guided by the rigidity of the substrate Biophys J 79 144 152 10866943 10.1016/S0006-3495(00) 76279-5 1:CAS:528:DC%2BD3cXks1Klurc%3D (Pubitemid 30436733)
42. Y Luo GL Radice 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 1479 12640032 10.1242/jcs.00339 1:CAS:528:DC%2BD3sXjtlyrtLY%3D (Pubitemid 36527494)
43. MP Maddugoda MS Crampton AM Shewan AS Yap 2007 Myosin VI and vinculin cooperate during the morphogenesis of cadherin cell cell contacts in mammalian epithelial cells J Cell Biol 178 529 540 17664339 10.1083/jcb.200612042 1:CAS:528:DC%2BD2sXos1CrsLc%3D (Pubitemid 47196159)
44. T Matsuda K Takahashi T Nariai T Ito T Takatani Y Fujio J Azuma 2005 N-cadherin-mediated cell adhesion determines the plasticity for cell alignment in response to mechanical stretch in cultured cardiomyocytes Biochem Biophys Res Commun 326 228 232 15567175 10.1016/j.bbrc.2004.11.019 1:CAS:528: DC%2BD2cXhtVagsrvL (Pubitemid 39573223)
45. T Matsushita M Oyamada K Fujimoto Y Yasuda S Masuda Y Wada T Oka T Takamatsu 1999 Remodeling of cell-cell and cell-extracellular matrix interactions at the border zone of rat myocardial infarcts Circ Res 85 1046 1055 10571536 1:CAS:528:DyaK1MXns1Ontb8%3D
46. R McBeath DM Pirone CM Nelson K Bhadriraju CS Chen 2004 Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev Cell 6 483 495 15068789 10.1016/S1534-5807(04)00075-9 1:CAS:528:DC%2BD2cXjsFeqsbk%3D (Pubitemid 38456178)
47. RM Mege J Gavard M Lambert 2006 Regulation of cell-cell junctions by the cytoskeleton Curr Opin Cell Biol 18 541 548 16905303 10.1016/j.ceb.2006.08.004 1:CAS:528:DC%2BD28XpsVOjtLk%3D (Pubitemid 44349065)
48. F Monier-Gavelle JL Duband 1997 Cross talk between adhesion molecules: control of N-cadherin activity by intracellular signals elicited by beta1 and beta3 integrins in migrating neural crest cells J Cell Biol 137 1663 1681 9199179 10.1083/jcb.137.7.1663 1:CAS:528:DyaK2sXkt1yis7g%3D (Pubitemid 27282245)
49. DJ Mooney R Langer DE Ingber 1995 Cytoskeletal filament assembly and the control of cell spreading and function by extracellular matrix J Cell Sci 108 Pt 6 2311 2320 7673351 1:CAS:528:DyaK2MXmsFOnsr4%3D
50. CM Nelson DM Pirone JL Tan CS Chen 2004 Vascular endothelial-cadherin regulates cytoskeletal tension, cell spreading, and focal adhesions by stimulating RhoA Mol Biol Cell 15 2943 2953 15075376 10.1091/mbc.E03-10-0745 1:CAS:528:DC%2BD2cXks1yrt7g%3D (Pubitemid 38691881)
51. WJ Nelson F Drees S Yamada 2005 Interaction of cadherin with the actin cytoskeleton Novartis Found Symp 269 159 168 16358407 10.1002/047001766X.ch13 1:CAS:528:DC%2BD2sXoslGku74%3D discussion 168-177, 223-130
52. WJ Nelson R Nusse 2004 Convergence of Wnt, beta-catenin, and cadherin pathways Science 303 1483 1487 15001769 10.1126/science.1094291 1:CAS:528:DC%2BD2cXhslCgsbo%3D (Pubitemid 38314410)
53. KK Parker DE Ingber 2007 Extracellular matrix, mechanotransduction and structural hierarchies in heart tissue engineering Philos Trans R Soc Lond B Biol Sci 362 1267 1279 17588874 10.1098/rstb.2007.2114 1:CAS:528: DC%2BD2sXps1Sjt74%3D (Pubitemid 47195021)
54. KK Parker J Tan CS Chen L Tung 2008 Myofibrillar architecture in engineered cardiac myocytes Circ Res 103 340 342 18635822 10.1161/CIRCRESAHA. 108.182469 1:CAS:528:DC%2BD1cXptlKnu74%3D
55. RJ Pelham Jr Y Wang 1997 Cell locomotion and focal adhesions are regulated by substrate flexibility Proc Natl Acad Sci USA 94 13661 13665 9391082 10.1073/pnas.94.25.13661 1:CAS:528:DyaK2sXotValtro%3D (Pubitemid 28009639)
56. GL Radice H Rayburn H Matsunami KA Knudsen M Takeichi RO Hynes 1997 Developmental defects in mouse embryos lacking N-cadherin Dev Biol 181 64 78 9015265 10.1006/dbio.1996.8443 1:CAS:528:DyaK2sXmtlGmug%3D%3D (Pubitemid 27079635)
57. D Rhee JM Sanger JW Sanger 1994 The premyofibril: evidence for its role in myofibrillogenesis Cell Motil Cytoskeleton 28 1 24 8044846 10.1002/cm.970280102 1:STN:280:DyaK2czitVWntA%3D%3D (Pubitemid 24138655)
58. J Rhee T Buchan L Zukerberg J Lilien J Balsamo 2007 Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription Nat Cell Biol 9 883 892 17618275 10.1038/ncb1614 1:CAS:528:DC%2BD2sXosVSltL0%3D (Pubitemid 47190443)
59. D Riveline E Zamir NQ Balaban US Schwarz T Ishizaki S Narumiya Z Kam B Geiger AD Bershadsky 2001 Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism J Cell Biol 153 1175 1186 11402062 10.1083/jcb.153.6.1175 1:CAS:528:DC%2BD3MXktlOmsLc%3D (Pubitemid 34289257)
60. SA Ruiz CS Chen 2008 Emergence of patterned stem cell differentiation within multicellular structures Stem Cells 26 2921 2927 18703661 10.1634/stemcells.2008-0432
61. B Russell D Motlagh WW Ashley 2000 Form follows function: how muscle shape is regulated by work J Appl Physiol 88 1127 1132 10710412 1:CAS:528:DC%2BD3cXit1Wlur0%3D (Pubitemid 30154920)
62. AM Samarel 2005 Costameres, focal adhesions, and cardiomyocyte mechanotransduction Am J Physiol Heart Circ Physiol 289 H2291 H2301 16284104 10.1152/ajpheart.00749.2005 1:CAS:528:DC%2BD28XlslGgsQ%3D%3D (Pubitemid 41698534)
63. MA Schwartz 2009 Cell biology. The force is with us Science 323 588 589 19179515 10.1126/science.1169414 1:CAS:528:DC%2BD1MXhsVKksbY%3D
64. R Sepp NJ Severs RG Gourdie 1996 Altered patterns of cardiac intercellular junction distribution in hypertrophic cardiomyopathy Heart 76 412 417 8944586 10.1136/hrt.76.5.412 1:STN:280:DyaK2s7gtVSiuw%3D%3D (Pubitemid 26390797)
65. SY Shai AE Harpf CJ Babbitt MC Jordan MC Fishbein J Chen M Omura TA Leil KD Becker M Jiang DJ Smith SR Cherry JC Loftus RS Ross 2002 Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure Circ Res 90 458 464 11884376 10.1161/hh0402.105790 1:CAS:528:DC%2BD38XitFGgt78%3D (Pubitemid 34633916)
66. AM Shewan M Maddugoda A Kraemer SJ Stehbens S Verma EM Kovacs AS Yap 2005 Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts Mol Biol Cell 16 4531 4542 16030252 10.1091/mbc.E05-04-0330 1:CAS:528:DC%2BD2MXhtVygtL7K (Pubitemid 41416439)
67. A Skwarek-Maruszewska P Hotulainen PK Mattila P Lappalainen 2009 Contractility-dependent actin dynamics in cardiomyocyte sarcomeres J Cell Sci 122 2119 2126 19470580 10.1242/jcs.046805 1:CAS:528:DC%2BD1MXovFens7k%3D
68. JC Sparrow F Schock 2009 The initial steps of myofibril assembly: integrins pave the way Nat Rev Mol Cell Biol 10 293 298 19190670 10.1038/nrm2634 1:CAS:528:DC%2BD1MXhtlyit7s%3D
69. Tabdanov E, Chopra A, Janmey P, Kresh JY (2010) The multi-cellularly coordinated myocyte cytoskeleton self-reorganization in response to self-generated stress fields. 5th International Workshop on Cardiac Mechano-Electric Coupling and Arrhythmias 1-4 September Oxford, England, p 69
70. M Takeichi 1995 Morphogenetic roles of classic cadherins Curr Opin Cell Biol 7 619 627 8573335 10.1016/0955-0674(95)80102-2 1:CAS:528:DyaK2MXosVKnsr8%3D
71. M Thery A Pepin E Dressaire Y Chen M Bornens 2006 Cell distribution of stress fibres in response to the geometry of the adhesive environment Cell Motil Cytoskeleton 63 341 355 16550544 10.1002/cm.20126 1:CAS:528: DC%2BD28XlvF2gurs%3D (Pubitemid 43787719)
72. M Thery V Racine M Piel A Pepin A Dimitrov Y Chen JB Sibarita M Bornens 2006 Anisotropy of cell adhesive microenvironment governs cell internal organization and orientation of polarity Proc Natl Acad Sci USA 103 19771 19776 17179050 10.1073/pnas.0609267103 1:CAS:528:DC%2BD2sXjtVSrsQ%3D%3D (Pubitemid 46037506)
73. KT Tokuyasu AH Dutton B Geiger SJ Singer 1981 Ultrastructure of chicken cardiac muscle as studied by double immunolabeling in electron microscopy Proc Natl Acad Sci USA 78 7619 7623 6801654 10.1073/pnas.78.12.7619 1:STN:280:DyaL387ltV2hsw%3D%3D (Pubitemid 12186194)
74. JP Trinkaus JP Lentz 1964 Direct observation of type-specific segregation in mixed cell aggregates Dev Biol 89 115 136 14118782 10.1016/0012-1606(64) 90017-X 1:STN:280:DyaF2c%2Fns1Gitg%3D%3D
75. J Tsai L Kam 2009 Rigidity-dependent cross talk between integrin and cadherin signaling Biophys J 96 L39 L41 19289031 10.1016/j.bpj.2009.01.005 1:CAS:528:DC%2BD1MXnvVeqsLg%3D
76. Y Wang G Jin H Miao JY Li S Usami S Chien 2006 Integrins regulate VE-cadherin and catenins: dependence of this regulation on Src, but not on Ras Proc Natl Acad Sci USA 103 1774 1779 16446427 10.1073/pnas.0510774103 1:CAS:528:DC%2BD28Xhslehtrg%3D (Pubitemid 43228769)
77. T Yeung PC Georges LA Flanagan B Marg M Ortiz M Funaki N Zahir W Ming V Weaver PA Janmey 2005 Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion Cell Motil Cytoskeleton 60 24 34 15573414 10.1002/cm.20041 (Pubitemid 40066224)
78. AE Zemljic-Harpf JC Miller SA Henderson AT Wright AM Manso L Elsherif ND Dalton AK Thor GA Perkins AD McCulloch RS Ross 2007 Cardiac-myocyte-specific excision of the vinculin gene disrupts cellular junctions, causing sudden death or dilated cardiomyopathy Mol Cell Biol 27 7522 7537 17785437 10.1128/MCB.00728-07 1:CAS:528:DC%2BD2sXht1GltrjN (Pubitemid 350033658)